Ecology of Bivalves: An Ecosystem Approach (Marine Science Series)

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ECOLOGY OF MARINE BIVALVES AN ECOSYSTEM APPROACH

Richard F. Dame, Ph.D.

CRC Press Boca Raton New York London Tokyo © 1996 by CRC Press LLC

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Library of Congress Cataloging-in-Publication Data Dame, Richard F. Ecology of marine bivalves: an ecosystem approach/Richard F. Dame p. cm. Includes bibliographical references and index. ISBN 0-8493-8045-6 1. Hepatitis B virus. 2. Biology—molecular. I. McLachlan, Alan. II. Title. [DNLM: 1. Hepatitis B virus. QW 710 G289h] QR749.H64G78 1993 616′.0149—dc20 DNLM/DLC for Library of Congress

95-22620 CIP?

This book contains information obtained from authentic and highly regarded sources. Reprinted material is quoted with permission, and sources are indicated. A wide variety of references are listed. Reasonable efforts have been made to publish reliable data and information, but the author and the publisher cannot assume responsibility for the validity of all materials or for the consequences of their use. Neither this book nor any part may be reproduced or transmitted in any form or by any means, electronic or mechanical, including photocopying, microfilming, and recording, or by any information storage or retrieval system, without prior permission in writing from the publisher. The consent of CRC Press does not extend to copying for general distribution, for promotion, for creating new works, or for resale. Specific permission must be obtained in writing from CRC Press for such copying. Direct all inquiries to CRC Press, Inc., 2000 Corporate Blvd., N.W., Boca Raton, Florida 33431. © 1996 by CRC Press, Inc. No claim to original U.S. Government works International Standard Book Number 0-8493-8045-6 Library of Congress Card Number 95-22620 Printed in the United States of America 1 2 3 4 5 6 7 8 9 0 Printed on acid-free paper © 1996 by CRC Press LLC



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1

Ecosystem Perspective and Bivalve Molluscs

EVOLUTIONARY HISTORY The first bivalve molluscs appeared in the sea during the Cambrian period about 620 M years ago, or before organisms had invaded the land (Figure 1). Because their shells were made of calcium carbonate, bivalves are well represented in the fossil record and often used as paleontological markers. During the Paleozoic (620 to 230 M years ago), the bivalve molluscs were overshadowed by an unrelated but similarly structured group, the Brachiopods or lamp shells. Both groups were filter feeders and removed phytoplankton from the water column by means of a ciliary feeding mechanism. Gradually the bivalve molluscs increased in importance so that by the Mesozoic era they were dominant and remain so today (Yonge 1960). The basic bivalve plan has been successful for many hundreds of millions of years. Due to the similarities between some fossil forms and extant species, it has often been said that an oyster of 200 M years ago would be perfectly familiar if served in a restaurant today (Yonge 1960). The bivalve molluscs are thought to have originated in warm shallow euhaline coastal waters and gradually invaded estuaries and brackish systems, as well as all the reaches of the world ocean. Because the adult forms of the majority of these animals are benthic or bottom dwelling, many different evolutionary adaptations to the benthic habitat have occurred. The most common life styles are: buried within burrows in unconsolidated soft sediments; attached by byssal threads to pebbles or more consolidated sediments; cemented to shells or rocks; and as semimobile members of the epibenthos. Today these adaptations are exemplified by clams, mussels, oysters, and scallops, respectively. In nature there are often gradients of sediments from muddy unconsolidated materials to hard substrates that reflect a water dynamics-energy gradient from low energy to high energy environments, with bivalves zoned accordingly (Morton 1992). As dense associations of bivalves are likely to have the greatest influence on their ecosystems, when and where did reefs and beds of these organisms appear? Primitive and long extinct bivalves, the rudists, appeared in the Paleozoic (Figure 2). They were gregarious in nature and were often found in association with corals and other reef-forming organisms (Stenzel 1971). Later, the fossil gryph-shaped oysters of the Miocene are often found associated with corals and other euhaline reef-building forms. This suggests that the advantages of reef building were exploited by bivalves at an early stage in their evolution.

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FIGURE 1. Evolutionary history of bivalve molluscs. (Data from Yonge 1960, Stenzel 1971, and Morton 1992.)

FIGURE 2.

Rudist reef. (Adapted from Kauffman and Sohl 1974.)





The largest reef building bivalve known was Crassostrea gryphoides, the giant oyster, also known as C. gigantissima, in North America. These bivalves with a reported height of 60 cm, weight of 4.5 kg, and shell thickness of 15 cm grew rapidly in the warm shallow brackish waters of the Miocene (Stenzel 1971). Today, bivalve reefs are only formed by brackish water species such as Crassostrea and Mytilus. In contrast to coral reefs, these reefs are found mainly in the temperate zone (Hughes 1991). In most cases, as the bivalve shell framework accumulates, it eventually becomes unstable and collapses. However, in the southeastern U.S.A., oyster reefs dominated by C. virginica can reach extensive size and persist for long periods of time (Hughes 1991). The first clear attempt relating living bivalves to their associated organisms and physical environment was by Möbius (1880). In his studies of oyster beds along the Schleswig-Holstein shore of Germany and the estuaries of England, he noticed that the organisms found there had numerous things in common. First, the same species composition of bivalves, crabs, barnacles, bryozoans, starfish, sea urchins, worms, fish, and algae were present. Möbius speculated that every oyster bed is a collection of organisms that find everything necessary for their growth and reproduction. Second, these organisms were normally found with similar environmental qualities of food, salinity, temperature, and substrate. He coined the word “bioceonosis” to describe the community of living organisms that are mutually limited by the environment. Möbius also observed that when the external environment changed, so did the composition of the bed. This effective binding of the community of organisms to the vagaries of the environment is a strong predilection toward what today we think of as ecosystems.

ECOSYSTEMS Ecosystems are organized assemblages of plants and animals in complex interaction with each other and their physical environment. While individual species are governed by genetic and physiological processes, their existence in nature is conditioned by the total environment and in turn influences the environment of which they are a part. Because of such complex interdependencies, understanding ecosystems requires studies that holistically elucidate principles of total system function. For the purposes of this book, I will use Odum’s (1983) definition for ecosystems: an ecosystem is any unit that includes all organisms that function together in a given area interacting with the physical environment so that the flow of energy leads to clearly defined biotic structure and cycling of materials between living and non-living parts.

Within the ecosystem approach, the structural components of biomass (including skeleton), hierarchy, food webs, flow networks, and biodiversity are important in determining the role of bivalves in ecosystems. Energy flow and material cycling processes, e.g., feeding, respiration, growth, excretion, and predation, as well as control by feedback loops, all help describe the functional roles bivalves play within





marine and coastal ecosystems (Figure 3). Quite often the magnitude of functional processes is closely coupled to the biological and physical aspects of structure.

FIGURE 3. Functional processes of bivalve systems.

STRUCTURAL ATTRIBUTES The most obvious and tangible contribution of bivalves to the structure of ecosystems is the biomass, skeleton and burrows of the animals themselves. The shells of bivalves not only provide a platform for these animals, but when taken with the soft body, amount to major components within some ecosystems. These structures also form a system matrix within which habitats are generated for other organisms. This matrix allows an increase in species diversity and leads to increased system complexity and redundancy (Hughes 1991). The physical environment is also a component of ecosystem structure. Not only can abiotic factors limit the abundance and extent of the biota, but the living components can influence the physical environment. Because bivalve shells are rigid, the flow of water around them can be both microscopically and macroscopically altered. In dense associations of bivalves in the form of reefs or beds, the accumulated empty and living shells of bivalves can markedly alter the physical dynamics of water flow over these structures at even greater physical scales, i.e., creek or channel. Generally, the orientation of the individual bivalves within the bed tends to enhance water circulation and turbulence over the system and in turn enhances the functional performance of the molluscs (Hughes 1991).

SYSTEM HIERARCHY Recently, the development and application of the ideas of levels of spatial and temporal organization, now known as hierarchy theory, have blossomed in ecosystem ecology (O’Neill et al. 1986). These authors note that the relationships between the © 1996 by CRC Press LLC




organisms in a system and the functions of the system are not always clear. They contend that hierarchy theory provides a framework for understanding this relationship without reducing one area of emphasis to the other. Two separate hierarchies, the population–community and the process–functional approaches, have emerged, which address ecosystems differently. The former is based on like taxonomic groupings, while the latter is predicated on similar ecological processes. Essentially, the two different fields view the natural world from different observational perspectives. The population–community approach is tangible and envisions a sequence of ORGANISM–POPULATION–COMMUNITY (Figure 4) and this hierarchy generally views the physical environment as a backdrop to the biological processes (O’Neill et al. 1986). The process–functional school places organisms of like functional roles together (Figure 4) with the functional group at the base and the biosphere at the top (O’Neill et al. 1986). This hierarchy is less tangible than the population–community hierarchy, but the physical environment is interwoven conceptually.

FIGURE 4.

Simple hierarchies in ecosystems. (Adapted from O’Neill et al. 1986.)

There is no immediately recognizable one-to-one or even many-to-one correspondence between the two hierarchies (O’Neill et al. 1986). Generally, components of neither of the two hierarchies can be reduced to each other in any simple way. It is also well known from observations of functional redundancy that many species can perform essentially the same ecosystem task. It is also probable that changes in the biodiversity of a system can in some cases influence ecosystem function. Further, many ecosystem functions, i.e., nutrient cycling, involve components that are abiotic (e.g., sediments) or combine biotic and abiotic elements. Obviously there is no easy correspondence of such components with species or assemblages of species. Often the population–community and process–functional hierarchies are difficult to rectify with each other. However, in some ecosystems, a single species or a group of closely related species may dominate a process or functional component. In such cases, there is a direct correspondence between the population–community and process–functional hierarchies (Figure 5). A classical example is the former dominance of a single population of large ungulate herbivores, bison, in the extensive grassland ecosystems of North America. Likewise, in estuaries, extensive populations of mussels or oysters will dominate the herbivore component of these shallow © 1996 by CRC Press LLC




water ecosystems and provide a potentially useful correspondence between the two hierarchies (Dame 1993).

FIGURE 5. Correspondences between population–community and process–functional hierarchies in bivalve-dominated systems.

FOOD WEBS Food energy or matter is transferred through the organisms that make up an ecosystem, and the interlocking relationships between the various biological components provide structure to the ecosystem and are called a food web. Description of the components and the relationships between them is a long-held aspect of ecology. Only recently have issues arisen concerning the influence or control, both quantitative and qualitative, of particular components on their food web. Initially these questions were solely from the population–community perspective, but recently a broader ecosystem perspective appears to be emerging. The paradigm of bottom-up control of food chains (Figure 6), with nutrients and light of major importance to primary producers and resulting material flows up the food chain to affect the remaining trophic levels, is well founded historically (Lindeman 1942). The top-down (cascading) or food chain dynamics theory was first proposed by Hairston et al. (1960) and was recently more fully developed by Fretwell (1987) and Oksanen (1988). This theory predicts that the top predator controls the next lower trophic level, resulting in alternating magnitude (negative correlation) of biomass and turnover patterns for adjacent trophic levels. Many of the speculations concerning bivalve filter feeders controlling phytoplankton abundances in the water column subtly fall into this category. The mutualism–cybernetics theory of Odum and Biever (1984) suggests that plant–herbivore interactions are typically donor controlled or mutualistic (positive © 1996 by CRC Press LLC




FIGURE 6. Food chain controls using energy symbols.

correlation), as herbivores often stimulate the production of the plant species that they feed on. The latter theory is favored by the process–functional group, but attacked by the population–community ecologists because it implies community selection or evolution above the species level. Because of these criticisms, Vadas (1989) has proposed another theory, the donor control–indirect effects theory. In this idea, species interact at ecological time scales with indirect effects caused by nutrient cycling, competition, and abiotic fluctuations leading to donor-controlled predator–prey interactions. More recently, Hunter and Price (1992) and Menge (1992) have argued in a similar vein that bottom-up and top-down controls operate simultaneously in most systems, and it is the net pattern that we observe in nature. I know of only two studies to date that address the food web control issue in ecosystems dominated by bivalves. In a mainly speculative vein, Menge (1992) has argued that both top-down and bottom-up controls operate simultaneously in shallow water systems coupled to the rocky intertidal zone along the Oregon coast. In these systems, the mussel, Mytilus, is a dominant component, and different scenarios are envisioned, depending on whether or not one system, Boiler Bay, is © 1996 by CRC Press LLC




driven by benthic plants (Figure 7) or the other, Strawberry Hill, is controlled by phytoplankton (Figure 8).

FIGURE 7. Hypothetical interaction food web for Boiler Bay, OR, with size of compartment indicating abundance and thickness of line indicating strength of relationship. (Adapted from Menge 1992.)

In a series of intense ecosystem level studies, Dame et al. (1989, 1991) investigated the role of oysters and mussels on material processing in estuaries. Utilizing a preliminary field experiment, Dame and Libes (1993) showed that the removal of oysters from a series of tidal creeks did not influence phytoplankton abundance as measured by chlorophyll a or water column primary production, but did significantly reduce the concentrations of dissolved inorganic nutrients. Thus these results within small creeks and on short time scales, imply a potential dominance of both bottomup and top-down controls within these systems.





FIGURE 8. Hypothetical interaction food web for Strawberry Hill, Oregon as described in Figure 7. (Adapted from Menge 1992.)

NETWORKS Food chains and webs are simple conceptualizations of natural ecological systems. In order to develop deeper understandings of the dynamics of ecosystems, ecologists have constructed much more complicated models. Some models have been designed for computer simulation and utilize systems of differential equations, while others are created for analysis. From a process–functional point of view, the measurement and depiction of material and energy flow between the various ecosystem components can show the efficiency with which material is transferred, assimilated, and dissipated. Such conceptualizations (see Chapter 7) convey considerable information on the structure of the ecosystem (Baird et al. 1991). Collectively known as network analysis, input–output, trophic, and cycle analysis have been applied in an engineer© 1996 by CRC Press LLC




ing sense to a number of bivalve-dominated systems, an oyster reef in South Carolina (Dame and Patten 1981), Chesapeake Bay (Baird and Ulanowicz 1993), and several less-studied systems (Baird et al. 1991).

BIODIVERSITY Diversity is inherent in all levels of biological organization, from the molecules that carry genetic information, to species where natural selection takes place, to ecosystems where organisms interact with each other and their environment. From this perspective, biodiversity is a fundamental property of the structure and function of ecosystems (Ray 1991). In a process–functional view, if the diversity of organisms changes within a system, it is not clear what will happen to the functional attributes of the system in question. Although a fair amount is known about the diversity of bivalve mollusc species through space and time, molecular diversity in bivalves is only known in a few commercially important species, and the role of bivalves in biodiversity and ecosystem function is relatively unknown.

FUNCTIONAL ATTRIBUTES At the ecosystem level, the most important functional processes deal with the flow of energy and cycling of materials between and within systems. Traditionally, groups of organisms with similar functions, processes, feeding, or trophic levels have been grouped together into functional components. The most common functional groups represented by bivalves are filter feeders, deposit feeders, consumers, and herbivores. Each component has inflows and outflows that are represented by specific organismic level processes, e.g., feeding and excretion (Figure 3). As energy and matter are processed and transformed by the organisms, work is done and degraded energy or waste heat is lost from the system. This latter process is known as respiration at both the organismic and system levels. Production or growth is the storage of energy and matter by a given system component. These processes may result in the increase in size of individuals or populations of animals over a unit of time. Predation is the removal of energy and materials by one component feeding on another, usually animals eating animals. The activity of herbivores eating plants or grazing may also be termed predation. Nutrient cycling is the process of specific types of nutrients or molecules moving from component to component within the ecosystem. Since matter is finite, atoms are used and reused within the ecosystem and the rates at which this reuse takes place is an exceedingly important process in ecosystem ecology. By determining nutrient cycling pattern and rates, ecosystems can be compared and important components in the cycling of a particular nutrient within ecosystems can be identified. In some ecosystems, bivalves are thought to increase the rate of nutrient cycling because of their high abundances and high metabolic rates (Table 1).

SYSTEM TYPES A variety of bivalve molluscs are prominent members of many diverse marine systems (Figure 9). These animals have reached their greatest abundances in shallow © 1996 by CRC Press LLC




TABLE 1 Spatial and Temporal Scales for Processes Involving Bivalve Molluscs Process

Spatial Scale

Physiological Predation Associations Disease Temperature–salinity Storms Epidemics Climate change

cm–m 1–10 cm 1–10 cm cm–km 1–100 km 1–100 km 10–1000 km Global

Duration Minutes Minutes–hours Days Days–weeks Days Days Years 10–100,000 years

Frequency None–seasonal Weeks–months Months–years Months–years Months–decades Decades–centuries 10,000–100,000 years

coastal waters and estuaries. In these systems, phytoplankton is consumed from tidal waters sweeping over dense beds of bivalves, mainly clams, cockles, mussels, oysters, and scallops. The dominant bivalves in these systems are adapted to changing temperatures and salinities and some are adapted to exposure and wave action in the intertidal zone. Three different life styles are prevalent: gregarious permanently attached forms, oysters; gregarious byssally attached and partially mobile forms, mussels; and bivalves that burrow into semi- or unconsolidated sediments, clams. Some bivalves have been successful in the extreme environments of the rocky intertidal zone and the sandy beach. In the former, rapid growth and a protective shell are major attributes, while in the latter, rapid burrowing in shifting sediments is important. In the low productivity zones of coral reefs and the deep sea vents, endosymbiotic relationships allow bivalves to succeed. Finally, shipworms succeed with specialized functions in eating and decomposing woody debris washed into the sea from the land.

REMAINING CONTENTS Having presented a broad ecological setting, the remainder of this book focuses on the specific attributes of bivalve molluscs that allow them to play an important role in marine ecosystems. This presentation does not address bivalve genetics (see Gosling 1992 for an introduction) or aquaculture (see Menzel 1991 for a review) specifically, but there are many implicit references to the latter. Using the classical ecosystem approach, the interactions of bivalves with the physical environment, particularly temperature, salinity, and water motion are reviewed first. These interactions can have a major influence on rate processes or functions at the organismic level. Thus, the roles of filtration, respiration, growth, and reproduction are examined from an ecosystem perspective. Population and community scale interactions are addressed with particular attention given to growth, predation, and refugia in the well-studied mussel and oyster systems. The ecosystem process of bivalves grazing on primary producers is considered, and the potential for bivalves to control primary production is carefully examined. Intimately related to primary production, metabolism and nutrient cycling are described for several systems to define the role of © 1996 by CRC Press LLC




FIGURE 9. Trophic groups of some common bivalves: (A) filter feeders (adapted from Barnes 1974); (B) deposit feeder; (C) photoautotroph or photosymbiotic giant clam (adapted from Lucus 1988); (D) chemoautrotroph or chemosymbiotic mussels (adapted from Fisher 1990).

bivalves as potential high speed processors of reactive nutrients. Because the sum of the preceding processes is exceedingly complex, some of the major conceptual and computer simulation models in which bivalves play a central role are reviewed. As it is difficult to test hypotheses only with models, ecosystem scale experiments © 1996 by CRC Press LLC




are described with their inherent strengths and weaknesses. Recognizing that marine bivalves are proven monitors and indicators of ecosystem stress, their role in ecosystem health is summarized. In the final chapter, the various aspects of bivalves in ecosystems are drawn together and the areas of most pressing research need are restated.

REFERENCES Baird, D., McGlade, J.M., and Ulanowicz, R.E. 1991. The comparative ecology of six marine ecosystems, Phil. Trans. R. Soc. Lond. Ser. B, 333, 15–29. Baird, D. and Ulanowicz, R.E. 1989. The seasonal dynamics of the Chesapeake Bay, Ecol. Monogr., 59, 329–364. Barnes, R.D. 1974. Invertebrate Zoology, 3rd ed., Saunders, Philadelphia, 870 pp. Dame, R.F. 1993. The role of bivalve filter feeder material fluxes in estuarine ecosystems, in Dame, R.F., Ed., Bivalve Filter Feeders and Coastal and Estuarine Ecosystem Processes, Springer-Verlag, Heidelburg, 245–269. Dame, R.F., Dankers, N., Prins, T., Jongsma, H., and Smaal, A. 1991. The influence of mussel beds on nutrients in the Western Wadden Sea and Eastern Scheldt estuaries, Estuaries, 14, 130–138. Dame, R.F. and Libes, S. 1993. Oyster reefs and nutrient retention in tidal creeks, J. Exp. Mar. Biol. Ecol., 171, 251–258. Dame, R.F. and Patten, B.C. 1981. The analysis of energy flows in an intertidal oyster reef, Mar. Ecol. Prog. Ser., 5, 115–124. Dame, R.F., Spurrier, J.D., and Wolaver, T.G. 1989. Carbon, nitrogen, and phosphorus processing by an oyster reef, Mar. Ecol. Prog. Ser., 54, 249–256. Fisher, C.R. 1990. Chemoautotrophic and methanotrophic symbioses in marine invertebrates, Rev. Aquat. Sci., 2, 399–436. Fretwell, S.C. 1987. Food chain dynamics: the central theory of ecology?, Oikos, 50, 291–301. Gosling, E.M. 1992. Genetics of Mytilus, in Gosling, E., Ed., The Mussel Mytilus, Ecology, Physiology, Genetics and Culture, Elsevier, New York, 309–382. Hairston, N.G., Smith, F.E., and Slobodkin, L.B. 1960. Community structure, population control, and competition, Am. Nat., 94, 421–424. Hughes, R.N., 1991. Reefs, in Barnes, R.S.K. and Mann, K.H., Eds., Fundamentals of Aquatic Ecology, Blackwell Scientific, Oxford, 213–229. Hunter, M.D. and Price, P.W. 1992. Playing chutes and ladders: heterogeneity and the relative roles of bottom-up and top-down forces in natural communities, Ecology, 73, 724–732. Kauffman, E.G. and Sohl, N.F. 1974. Structure and evolution of Antillean Cretaceous rudist frameworks, Verh. Naturforsch. Ges., 84, 399–467. Lindeman, R.L. 1942. The trophic-dynamic aspect of ecology, Ecology, 23, 399–418. Lucus, J.S. 1988. Giant clams: description, distribution and life history, in Copland, J.W. and Lucas, J.S., Eds., Giant Clams in Asia and the Pacific, Australian Center for International Agricultural Research, Canberra, 21–32. Menge, B. 1992. Community regulation: under what conditions are bottom-up factors important on rocky shores?, Ecology, 73, 755–765. Menzel, W. 1991. Estuarine and Marine Bivalve Mollusk Culture, CRC Press, Boca Raton, FL, 362 pp. Möbius, K. 1880. Die Auster und die Austerwirthschaft, Rep. U.S. Comm. Fish., 683–751.





Morton, B. 1992. The evolution and success of the heteromyarian form in the Mytiloida, in Gosling, E., Ed., The Mussel Mytilus, Ecology, Physiology, Genetics and Culture, Elsevier, Amsterdam, 21–52. Odum, E.P. 1983. Basic Ecology, Saunders, Philadelphia, 603 pp. Odum, E.P. and Biever, L.J. 1984. Resource quality, mutualism, and energy partitioning in food chains, Am. Nat., 124, 45–52. Oksanen, L. 1988. Ecosystem organization, mutualism and cybernetics or plain Darwinian struggle for existence?, Am. Nat., 131, 424–444. O’Neill, R.V., DeAngelis, D.L., Waide, J.B., and Allen, T.F.H. 1986. A Hierarchical Concept of Ecosystems, Princeton University Press, Princeton, NJ, 253 pp. Ray, G.C. 1991. Coastal-zone biodiversity patterns, Bioscience, 41, 490–498. Stenzel, H.B., 1971. Oysters, in Moore, R.C., Ed., Treatise on Invertebrate Paleontology, Part N, Mollusca 6, Bivalvia, Geological Society of America, Lawrence, KS, N593–1051. Vadas, R.L. 1989. Food web patterns in ecosystems, a reply to Fretwell and Oksanen, Oikos, 56, 339–343. Yonge, C.M. 1960. Oysters, Collins, London, 209 pp.





2

Physical–Environmental Interactions

INTRODUCTION From an ecosystem perspective, the biotic and abiotic components of a given environment are intimately bound together to control and generate the ecological system. In many instances, there is a two-way interaction: the physical environment may control living components and the biotic environment may control abiotic components. The existence of an organism in a given environment implies that the organism has succeeded or survived in the presence of all the abiotic and biotic influences that impinge upon it. Any condition or factor that approaches or exceeds the organism’s tolerance for that factor is defined as a limiting factor or condition (Odum 1983). Studies on the lower limits of an organism’s existence to physical factors were initiated by Liebig (1847) and later formalized into Liebig’s “Law of the Minimum.” From Liebig’s studies, it was found that the law was strictly applicable only to systems in steady-state, i.e., systems where inflow balances outflow of energy and materials. In addition, Liebig found that factors or conditions can influence each other, and care must be taken to recognize this potential interaction. Organisms have a life zone, often called the “biokinetic zone” (Vernberg and Vernberg 1972), where there are both lower (minima) and upper limits for a given factor. This concept was first developed by Shelford (1913) and is generally termed Shelford’s “law of tolerance.” Organisms with broad ranges of tolerance to a given condition are termed “eury-,” while those with narrow biokinetic zones are called “steno-” (Figure 10). In the remainder of this chapter, the major abiotic environmental factors that influence bivalve molluscs will be reviewed. The focus will be on the so called “operationally significant” factors that play a major role on bivalves during their life cycles.

TEMPERATURE Temperature is a measure of the degree of random motion or kinetic energy in molecules of matter. Temperature not only limits the spatial distribution of bivalves, but also is a major controlling factor in many physiological rate processes, e.g., feeding and growth, that play important roles in many ecosystem level processes. Because bivalve molluscs produce only small amounts of heat during metabolism, they are termed “poikilotherms,” or animals whose body temperature conforms to





FIGURE 10. The generalized influence of temperature on rate processes in stenothermal and eurythermal bivalves. (Adapted from Shelford 1913.)

that of the environment. The majority of marine bivalves live within a temperature range from near –3°C to +44°C (Vernberg and Vernberg 1972). At the extremes, for example, intertidal oysters, Crassostrea, may attain body temperatures of 49°C in warm subtropical and tropical climates (Galtsoff 1964), and Mytilus in Canada have been shown to survive temperatures as low as –16°C (Bourget 1983), while coastal and estuarine bivalves tend to be eurythermal and oceanic forms are typically stenothermal in tolerance (Figure 10). Incident light input per unit area of surface decreases from the equator to the poles due to the curvature of the earth. This decrease in input energy results in a latitudinal temperature gradient of decreasing temperature with increasing latitude. The gradient in temperature may result in broad geographical zonation of bivalve species. For example, along the Atlantic coast of North America Mytilus edulis is common to Cape Hatteras at the southern limit of Virginia and absent south of that location. It is generally believed that the warm water, northward-moving currents (the Gulf Stream), so typical of the western boundaries of oceans, provide a temperature barrier to the distribution and survival of Mytilus larvae southward. In contrast, C. virginica is a more eurythermal species and is found over a broader latitudinal range both north and south of Cape Hatteras. It is important to note, as with many other species, that it is the tolerance of the mobile larval stage or reproductive period that is most sensitive to temperature. In addition to geographical distribution, physiological rates may vary over a latitudinal gradient. Butler (1953) has shown that for C. virginica growth rate of soft body is greatest near the central portion of this species’ north–south range, or about the location of Chesapeake Bay (Figure 11). North and south of that point growth rate declines. Along the coast of the Gulf of Mexico, Butler speculates that the oysters are near the limit of their geographical distribution. Excluding nongrowth months, Butler’s observations suggest that oysters from the warmest areas produce the least amount of biomass per unit time, and all other regions are considered





FIGURE 11. The influence of environmental temperature on the growth rate of Crassostrea virginica along a latitudinal gradient. (Data from Butler 1953.)

intermediate in growth rate. His data appear to fit the general form of the curve in Figure 10. Butler’s findings imply a more general application of perturbation theory and the subsidy-stress gradient approach (Odum et al. 1979). In this application, the input perturbation, temperature, is an energy source and a convex performance curve may simulate the system response (Figure 12). For the oyster case, as temperature increases, growth rate may increase and then gradually decrease. In addition, the relative variability of observed growth rate will increase as temperature increases. If the perturbation is destructive, as high temperatures are, then performance may be reduced to the point where the species and the community are replaced with more tolerant forms. In addition to latitudinal temperature gradients, subtropical, temperate, boreal, and arctic coastal water habitats experience seasonal cycles in temperature. Seasonality is caused by the inclination of the earth as it spins on its axis in relation to the sun. For bivalves, seasonality reaches its greatest extent in temperate and boreal shallow tidal waters where land–sea interactions have their greatest influence on temperature. Because organisms experience quite different temperature regimes depending on the time of year, they are essentially thermally acclimated to the different conditions in different seasons. Thermal acclimation is defined (Crisp and Ritz 1967) as any nongenetic adjustment by an organism in direct response to a change in a single factor in the environment. Many physiological rates, i.e., growth, respiration, feeding, excretion, etc., respond to thermal acclimation. In the case of intertidal oysters (Dame 1972), C. virginica, clearly respiration is significantly different at different acclimation temperatures (Figure 13). Thus, an organism can be seasonally





FIGURE 12. The general form of the subsidy-stress gradient approach and its similarity to oyster growth across a latitudinal gradient. (Modified from Odum et al. 1978.)

FIGURE 13. The influence of temperature on the respiration rates of intertidal American oysters, Crassostrea virginica. (Adapted from Dame 1972.)

acclimated to a temperature regime and be exposed to a variety of temperatures during a tidal or daily cycle. Physiological ecologists have approached this situation





by acclimating organisms to a series of temperatures and then observing physiological rates over a range of temperatures for a given acclimation temperature. Initially, only a single environmental factor and a specific physiological rate were observed, but now balanced energy budgets are developed for a target species (Kuenzler 1961 and Dame 1972) and integrated into population level estimates. Recent work has emphasized the combined effects of complex environmental variables on the integrated physiological response of the organism as a whole. This multidimensional approach, often called “response-surface analysis” (Alderdice 1972), has been applied to a number of bivalves including Mytilus (Widdows 1978; Bayne and Scullard 1978) and Ostrea (Buxton et al. 1981). In the case of Ostrea (Buxton et al. 1981), multiple linear regression analysis was used to obtain polynomial expressions for assimilated ration as a function of acclimation temperature and exposure temperature and respiration of the general form Y = a + bX1 + b2 X 2 K

and these relationships generated a 3-dimensional response surface. In summary, temperature is a major physical factor that limits the physical extent of bivalves both latitudinally and vertically. This abiotic parameter also influences ecosystems by controlling functional processes, such as survival, growth, feeding, and excretion. As temperature is seasonal in all but equatorial and deep sea habitats, this factor induces a considerable amount of temporal variation on bivalves and their ecosystems.

SALINITY While temperature is generally recognized as the principal factor at large biogeographic scales, salinity is an important determining factor in the distribution of coastal and estuarine bivalves and is influential on many physiological rates. Salinity may affect the structural and functional properties of animals through changes in (1) total osmotic concentration, (2) relative proportions of solutes, (3) coefficients of adsorption and saturation of dissolved gases, (4) density and viscosity (Kinne 1964). Although salt concentrations or salinities are fairly constant in the oceans at about 35‰, in coastal and estuarine regions salinity varies along a gradient from freshwater in landward areas to full marine salinity. Depending on the geographical location, salinity may vary seasonally due to seasonal river input and freshwater runoff and precipitation. Bivalve molluscs are found at all salinities including freshwater and hypersaline areas typical of tropical zones. Because estuarine and coastal species are not uniformly distributed across these salinity gradients, numerous schemes have been developed to describe the observed distributions (Bulger et al. 1993). The Remane and Schlieper scheme has been criticized because its database came from the Baltic Sea and probably incorporates a temperature gradient as well as a salinity gradient. However, the latter scheme was documented by Khlebovich (1969) to describe the principle of critical salinity.





This principle states that there is a salinity barrier between 5 to 8‰. Above this barrier, poikiloosmotic organisms can survive, but below the barrier, hyperosmotic regulation is required. Thus, this scheme is physiologically based. The most well-known scheme is the Venice system (Anonymous 1959). The Venice system was constructed from the experiences of the scientists of the day and has no reported objective criteria. The Bulger scheme supports the Venice system, but is based on field data and principal component analysis. The Bulger scheme divides the salinity gradient into the following overlapping zones: 0–4, 2–14, 11–18, 16–27, and 24–marine ‰. At the system or community level, Wells’ (1961) study of the fauna of oyster beds along a salinity gradient clearly demonstrates the influences of salt concentrations. Utilizing a series of nine stations along a 10-mile stretch of the Newport River estuary in North Carolina, Wells found a consistent decline in animal species in the oyster beds from over 60 species at the most saline station to less than 10 species at the most upstream site with salinities less than 10‰. Wells supported his field observations with a laboratory examination of low salinity tolerance by the 20 most common animal species found on these beds, including the bivalves Crassostrea, Mercenaria, Geukensia, Brachidontes, and Chione. A comparison of salinity death points and distribution along the salinity gradient resulted in a more or less similar ranking for the bivalves and all but two of the other animals. From these results, Wells concluded that a great majority of the species on the oyster bed are limited in their upstream distribution or penetration by salinity. Salinity also influences many of the major rate processes in bivalves, although laboratory and field studies do not always appear to agree (Bayne et al. 1976). Typically, the respiration rates of euryhaline bivalves are similar when measured at their field-ambient salinities (Remane and Schlieper 1971), but major differences occur when there is an acclimation period. Some of this discrepancy may be due to the necessity for a much longer acclimation period for salinity as opposed to the normal 2-week period for temperature acclimation (Bayne et al. 1976). Changes in environmental salinity may disrupt the steady-state balance between the input and output of cellular water and salts (Hawkins and Bayne 1992). Most bivalves respond immediately to changes in their environment by closing their shells and isolating themselves from the external salinity environment. This isolation helps to reduce the rate of associated changes in cell volume and allows isoosmotic intracellular regulation to commence (Hawkins and Bayne 1992). Thus, following a sudden change in salinity, physiological rates of feeding and respiration are depressed, but gradually the animal regains normal function. As with temperature, salinity can vary along a spatial gradient, particularly in coastal regions. Temporal variation may also occur due to precipitation and landwater runoff, but these variations are not as obvious as those noted for temperature. Like temperature, salinity limits the distribution of bivalves and can control the basic physiological rates that translate to functional processes in ecosystems.





TEMPERATURE–SALINITY AND OTHER FACTOR COMBINATIONS From the preceding discussion, it is evident temperature and salinity are significant abiotic factors that have major influences on biological processes. These two factors are often correlated in various ways. Temperature can modify the effects of salinity and enlarge, narrow, or shift the salinity range of an individual, and vice versa (Kinne 1964). The larvae and adults of bivalves are two distinct morphological and physiological organisms that occupy very different ecological environments (Lough 1974). Because of their coastal and estuarine water column environment, the larvae of most coastal bivalves experience great variations in temperature and salinity during their life stage. Using the response surface approach of Alderdice (1972), Lough (1974) compared the survival and growth of the early and late stage larvae of C. virginica, M. mercenaria, and Mulinia lateralis to the combined influences of temperature and salinity. Although the three species are euryhaline as adults, their larvae have a comparatively narrow salinity range. The observed progressive change in temperature–salinity tolerance with age or time approaches the range tolerated by the adults. Maximum predicted growth occurred at higher temperatures and somewhat higher salinities than those for maximum survival in all three species. Late larval survival and growth appear to be maximized to take advantage of the complex environment the larvae experience on approaching settlement. As bivalves move from one ecosystem to another during their larval stage, it is important that those interested in the whole system be aware of this spatial transition and the role continuously varying abiotic factors may play. The adult stage of most euryhaline bivalves is usually sessile or semisessile, and the animals must experience many potentially lethal or deleterious abiotic environmental stresses. Not only do temperature and salinity vary, but oxygen and other related chemical parameters may also impact on bivalve survival and physiological rates. For example, Shumway and Koehn (1982) show the effect of declining oxygen tension on the respiration of C. virginica adults at different temperatures and salinities, also using the response surface technique. Regulation of respiration in declining oxygen tension decreases with decreasing salinity and increasing temperature. Maximum respiration occurs at moderate salinity and 30°C at all oxygen tensions. In the case of C. virginica, this bivalve appears to have a rather “elastic” or “euryplastic” (Alderdice 1972) physiological ecology that allows it to utilize available oxygen over a broad range of temperature–salinity–oxygen combinations without falling into anaerobiosis. In other words, these oysters are well adapted to life in their constantly varying environment. The interaction of the two factors, temperature and salinity, with various bivalve processes can often describe the potential habitat of a given animal. It is also clear that because of the great differences in the benthic vs. the water column the adult bivalve responses to the physical parameters of temperature and salinity are different from those of the larvae of the same species. These life history differences allow





bivalves to exploit and exist in different ecosystems and, thus, increase their chance of survival and influence.

WATER MOVEMENT The interaction of moving water with bivalves has only recently been recognized as an important phenomenon. Most water flow is created by currents, usually tidal or wind driven, but on open shores or in shallow open bays water flow can also be generated by wave action. Filter feeding bivalves require sufficient water motion to bring in new supplies of suspended food and take away waste. In contrast, deposit feeding bivalves require low water flow to allow the accumulation of deposited seston as a food resource. In this view, the flowing water provides an energy subsidy that allows sessile bivalves to utilize a particular habitat far beyond the ability of the adjacent water column to provide food. If filter feeding bivalves accumulate in large numbers, the structures created by their beds can greatly alter the flow environment and in turn allow bivalves to play a role in the hydrodynamics and development of certain systems. From an ecological perspective there are two fundamental flow regimes, laminar and turbulent flow. In laminar flow, all the fluid particles move more or less parallel to each other in smooth paths, and this motion is the same at both low and high scale flow. Turbulent flow is very different, with the fluid particles moving in a highly irregular manner even if the fluid as a whole is traveling in a single direction. The transition point between the two flow regimes is often abrupt and is also where biological processes are of major importance (Vogle 1981). The removal of momentum from a moving fluid by a body, i.e., a bivalve, is known as drag. Because living systems are not uniform objects, drag is difficult to predict for them. As it turns out, the Reynolds number (Re) is a valuable descriptor of not only drag, but also other aspects of fluids interacting with solids. The Re is a scaling parameter that spans the spatial scales of living systems from molecules to ecosystems. Its role is sometimes comparable to that of the surface-to-volume ratio in physiology (Vogel 1981). Early studies showed that increasing fluid speed, increasing the size of the object in the flow, increasing the density of the fluid, and decreasing the viscosity of the fluid could shift a flow from laminar to turbulent. This combination of parameters derives the dimensionless Re. Re =

lU v

where l is the size of the object, U is the velocity of the fluid, and v the kinematic viscosity that is the ratio of the dynamic viscosity and density. The drag coefficient, CD′ describes the behavior of drag and is a function of the Re. Because most adult bivalves live on the bottom, it is water velocity near the bottom that is most ecologically important to these organisms. As water flows over the bottom, it is subject to frictional drag with the bottom that dissipates energy (momentum) in the flow and slows down the current. Therefore, at the interface © 1996 by CRC Press LLC




between the current and the bottom the velocity of the water is zero or near zero. The frictional effects of the bottom are transferred within the flow by molecular and turbulent mixing. Thus, there is a velocity gradient from near zero at the bottom to some distance above where the current is not significantly influenced by the bottom. This gradient is called the boundary layer (Figure 14). The boundary layer may be

FIGURE 14. A generalized diagram showing the influence of depth and water velocity on the different components of the boundary layer.

either turbulent or laminar. A laminar boundary layer is a region with very little exchange with the surrounding layers of water and often becomes depleted of nutrients and food, while accumulating waste materials. Laminar boundary layers are usually found at low water velocities, and turbulent layers are found at higher water velocities. Bottom roughness can enhance turbulent boundary layer formation and, thus, increase mixing within the current. In gradually varying flow regimes typical of uneven bottoms and changing water currents, the boundary layer can be divided into three layers (Frechette et al. 1993). Nearest the bottom is the viscous sublayer (Figure 14) where velocity varies linearly with height above the bottom. This layer is continuous and well defined over relatively smooth bottoms, but becomes discontinuous over rougher surfaces like mussel beds and oyster reefs. Under the latter conditions, the flow is said to be rough-turbulent and transport is largely determined by turbulent mixing processes. The next layer is the log layer where velocity varies logarithmically with distance above the bottom. The outermost layer is known as the defect layer and flow behavior here is largely independent of bottom roughness. Bivalves may respond to flowing water by orienting their shells to reduce drag and, thus, increase stability and increase the availability of food and removal of © 1996 by CRC Press LLC




waste. In sessile bivalves, it is well known that C. virginica living in high flow environments have elongated shells while those in low flow conditions have more rounded shells (Kauffman 1971). This observation implies a cause and effect relationship between water flow and structural morphology. The shell surface of many sessile bivalves is often rough with either uniform or nonuniform protuberances. This surface roughness may be an example of the “dimple” or “golf ball” phenomena described by Vogel (1981), where surface roughness induces the stability of an object in a current. From a slightly different perspective, Lawrence (1971) found that individual or isolated C. virginica in South Carolina showed little orientation to tidal currents, while densely packed or clustered animals on reefs oriented their planes of commissure parallel to water flow. He also found that fossil beds of Crassostrea gigantissima in North Carolina likewise oriented parallel to tidal flow. Not only do surface dwelling sessile bivalves orient to the flow, but siphonate infaunal bivalves do also. Vincent et al. (1988) noted that Mya arenaria usually orients normal to the axis of tidal flow over the clam flats. This orientation suggests that the preferred alignment minimizes the mixing of exhaled and inhaled water, thus optimizing filter feeding and reducing refiltration. From a system perspective, not only do bivalves respond to the boundary layer flow, but they also may also influence the boundary layer by pumping jets and siphon behavior (Monismith et al. 1980). From flume studies, Monismith et al. (1980) showed that a significant portion of excurrent water could be refiltered depending on the boundary layer velocity profile, velocity of the excurrent water and siphon height, orientation, and size. With nonsiphonate epifaunal mussels only the roughness generated by the shells appeared to influence turbulent mixing, and mussel pumping was not a necessary consideration to explain the observed velocity profiles (Frechette et al. 1993). In surface dwelling byssate and nonbyssate mobile bivalves, the animal tends to respond to a current by orienting the inhalant portion into the current and the exhalant area downstream. In addition, shell shape appears to influence the channeling of water across the bivalve from inhalant to exhalant areas. Evidence from flume experiments (Wildish et al. 1982, 1992) has clearly shown that forced orientation of the exhalant area of scallops into the current resulted in reduced growth and food uptake. Many scallops have developed jet propulsion or swimming as means of predator avoidance. This phenomenon is an adaptation of shell morphology and internal structure into an integrated behavior for survival. In this behavior, the bivalve not only utilizes the current, but because of its shell shape and jet propulsion generates lift and becomes an object moving through a fluid rather than just responding to the moving fluid (for more on this topic, see Wildish and Kristmanson 1993; Dadswell and Weihs 1990; Morton 1980). At a higher scale of organization, Grave (1905) hypothesized that oyster reefs build out from the shore towards the central channel. Later work by Keck et al. (1973) linked oyster reef development to tidal creek development. These workers found that reefs are often associated with large creek meanders where higher current velocities on the concave side of the bend result in areas of scour. The sediments





of this zone tend to be firm and swept free of soft mud and slime that are unsuitable for spat settlement. The convex side of the meander is an area of lower current velocities and a depositional zone for finer sediments and, thus, generally unsuitable for settlement and oyster survival. Once the reef has been established on the concave portion of the meander, the higher water velocities provide more food and carry away feces and pseudofeces. A recent study by Dame et al. (1987) noted that on a South Carolina oyster reef there was sufficient sediment deposition to cause burial within several tidal cycles. However, in this system maximum ebb tide water velocities over the reef were always adequate to resuspend the accumulated materials. In addition to structural effects, many functional processes are influenced by water movement. The most well studied of these relationships is the role of current speed on bivalve growth. In this process, it is assumed that the bivalves, particularly dense populations, reduce the concentration of suspended food in the overlaying boundary layer. Initially it was thought that the depletion of food from the boundary layer was a simple function of reduction in current speed (Wildish and Kristmanson 1984), and that this reduction in available food led to reduced growth. Later studies by Frechette et al. (1993) indicated that vertical mixing also plays a role. Depletion of the boundary layer can be alleviated by wave action or currents, but resuspension itself does not appear to positively affect the growth of mussels (Frechette and Grant 1991). Thus, it is appropriate that field observations of mussel beds of different sizes show higher mussel growth along the leading edges and reduced growth along the direction of flow and in the central portions of beds (Newell 1990). Waves are another form of water flow that influences bivalves. On rocky shores, many bivalves attach themselves to the substrate either through cementation or byssal threads. Although bivalves in these environments benefit from the seston produced by the wave-generated turbulent flows, there is some evidence (Harger 1971) that bivalves facing the direct ocean waves are not as large as those protected by boulders. These observations suggest that energy for growth may be diverted into repairing injuries sustained from more powerful waves. The role of wave energy in enhancing intertidal productivity has been examined along the northeastern Pacific by Leigh et al. (1987). These authors found that on shores with more wave energy productivity was higher. As intertidal organisms cannot transform wave energy into biochemical energy nor harness wave energy the real question is, how does this energy enhance productivity. Apparently, primary production is enhanced through numerous mechanisms: (1) increased primary production results in more food for animals like bivalves; (2) increased turbulence constantly renews the seston in the area of the bivalves, thus providing more food availability; and (3) wave action can protect residents of the intertidal zone by knocking away their enemies or preventing them from feeding. Bivalves living in current- and wave-dominated environments are the beneficiaries of increased food availability and waste removal, and these are essentially energy subsidies beyond normal solar inputs to ecosystems. Thus, in these environments it is very common to find large populations of bivalves that probably play major roles in the functioning of their respective ecosystems.





TIDES At the land–sea interface, tides have the potential to produce major effects on systems dominated by bivalves. The zone between the high and low tide marks is called the intertidal or littoral zone. Organisms in this zone are subject to exposure as the tide drops and submergence as the tide rises. During exposure, inhabitants are faced with increased temperature variability and increased desiccation. During submergence, temperature extremes are minimized and there is no desiccation, but in open areas, wave action can come into play by dislodging individuals or predators. Although the rise and fall of the tides tracks a smooth curve, zonation in the intertidal region is often attributed to tides. If a series of tidal curves is plotted, a series of distinct breaks is evident, and these breaks are thought to be related to the boundaries between zones. From Figure 15, showing maximum time of continuous submergence for various tide levels along the California coast, certain points or critical tide levels (Doty 1946) reflect sharp increases in exposure to air. These levels have been invoked to explain intertidal zonation. Support for the critical tide level explanation for zonation has been well accepted, most likely, because of the great variations in topography from place to place in the intertidal zone. Other mainly biological factors certainly play a role in intertidal zonation and these will be discussed in Chapter 4.

FIGURE 15. A diagram of critical tidal exposure levels along the California coast. (Redrawn after Doty 1946.)

At an ecosystem scale, tides allow the exchange of water between coastal environments. Thus, water molecules within coastal systems are constantly being replaced by other water molecules from either land runoff or the sea. The time it takes for all the molecules of water in a water mass to be replaced is called the turnover time. The time the average water molecule stays within a system is termed © 1996 by CRC Press LLC




the residence time. Turnover times range from hours to months, depending on tidal fluxes, land water inputs, and volume of the system. Short turnover times in the order of hours are typical of low volume systems or systems that go dry at low tide, while long turnover times are found in large volume seas and bays. The longer the turnover time the more time bivalves have to interact with the water volume. However, the biomass of bivalves now becomes an important factor in determining influence. High bivalve densities can offset the tidal dominance of rapid turnover times and lead to control of material turnover rates by these animals (Dame et al. 1992). In summary, tides can influence the spatial distribution of bivalves in coastal environments. Tides along with coastal geomorphology can determine the turnover time of coastal water volumes, and bivalve biomass can in some cases override the influence of tides in material transport.

SEDIMENTS Sediment composition is another physical parameter that seems to play a role in the spatial distribution of bivalves. Particle size, as catagorized into sand, silt and clay, is used to describe sediments. Often zones of low energy or little water flow are dominated by finer sediments while areas of high energy are composed of coarser sediments like sand. Since sediments and water flow are correlated, gradients of sediments are often found, particularly in coastal waters and in the intertidal zone. Generally, deposit feeding bivalves are prevalent in finer sediments, and filter feeding bivalves are common to coarser sediments (Rhoads and Young 1970). Although some of this bivalve spatial variation is due to local hydrodynamics and food availability, some is due to the specific species ability to live on the surface of changing sediments or burrow into the sediments. Because sediments are often in particle size gradients, it is not unexpected to find identifiable zones inhabited by different communities of bivalves in intertidal sands and muds (Peterson 1991). It has long been known that benthic suspension feeders and deposit feeders exhibit reciprocal spatial distributions. In environments where one type of bivalve is abundant and diverse, the other is reduced. Rhoads and Young (1970) found that deposit feeders, especially bivalves, intensively rework surface sediments and produce the following changes: (1) an uncompacted sediment consisting of fecal pellets and reworked material of semiconsoladated mud; (2) a surface of biogenic sandsize particles of low bulk density; and (3) sediments of high water content. These biological modifications of the sediment affect the physical stability of the bottom by increasing interface roughness and lowering critical erosion velocity. This physical instability of the surface sediments is proposed to be stressful to suspension feeding benthos (bivalves) by: (1) clogging filtering structures; (2) resuspending and burying newly settled larvae; and (3) discouraging the settlement of suspension feeding larvae. Unstable sediments also do not provide a suitable substrate for sessile filter feeding bivalves to attach to. Rhoads and Young (1970) further argue that this explanation is limited to areas of high primary production where food is not limiting to bivalve filter feeders. As noted earlier, Wildish and Kristmanson (1993) have observed that, in detailed velocity profile studies of similar habitats, it is the avail© 1996 by CRC Press LLC




ability of food for benthic suspension feeders in the benthic boundary layer that may be limiting their success. The size and composition of the benthic boundary layer are a result of current velocity, bottom composition, and biotic interactions.

REFERENCES Alderdice, D.F. 1972. Responses of marine poikilotherms to environmental factors acting in concert, in Kinne, O., Ed., Marine Ecology, Wiley, London, 1659–1722. Anonymous. 1959. Symposium on the classification of brackish waters, Venice, 8–14th April 1958, Arch. Oceanograf. Limnol., 11 (Suppl.) Bayne, B. L. and Scullard, C. 1978. Rates of oxygen consumption by Thais (Nucella) lapillus, J. Exp. Mar. Biol. Ecol., 32, 97–111. Bayne, B.L., Thompson, R.J., and Widdows, J. 1976. Physiology I, in Bayne, B.L. Ed., Marine Mussels: Their Ecology and Physiology, Cambridge University Press, New York, 121–206. Bourget, E. 1983. Seasonal variations of cold tolerance in intertidal mollusks and their relation to environmental conditions in the St. Lawrence Estuary, Can. J. Zool., 61, 1193–1201. Bulger, A.J., Hayden, B.P., Monaco, M.E., Nelson, D.M., and McCormick-Ray, M.G. 1993. Biologically-based estuarine salinity zones derived from a multivariate analysis, Estuaries, 16, 311–322. Butler, P.A. 1953. Oyster growth as affected by latitudinal temperature gradients, Commer. Fish. Rev., 15, 7–12. Buxton, C.D., Newell, R.C., and Field, J.G. 1981. Response- surface analysis of the combined effects of exposure and acclimation temperatures on filtration, oxygen consumption and scope for growth in the oyster Ostrea edulis, Mar. Ecol. Prog. Ser., 6, 73–82. Crisp, D.J., and Ritz, D.A. 1967. Temperature acclimation in barnacles. J. Exp. Mar. Biol. Ecol., 1, 236–256. Dadswell, M.J. and Weihs, D. 1990. Size related hydrodynamic characteristics of the giant scallop, Placopecten magellanicus, Can. J. Zool., 68, 778–785. Dame, R.F. 1972. The ecological energies of growth, respiration and assimilation in the intertidal American oyster, Crassostrea virginica, Mar. Biol., 17, 243–250. Dame, R.F. 1987. The net flux of inorganic matter by an intertidal oyster reef, Cont. Shelf Res. 7, 1421–1424. Doty, M.S. 1946. Critical tide factors that are correlated with the vertical distribution of marine algae and other organisms along the Pacific coast, Ecology, 27, 315–328. Frechette, M. and Grant, J. 1991. An in situ estimation of the effect of wind-driven resuspension on the growth of the mussel, Mytilus edulis, J. Exp. Mar. Biol. Ecol., 148, 201–213. Frechette, M., Lefaivre, D., and Butman, C.A. 1993. Bivalve feeding and the benthic boundary layer, in Dame, R.F., Ed., Bivalve Filter Feeders in Coastal and Estuarine Ecosystem Processes, Springer-Verlag, Heidelburg, 325–369. Galtsoff, P.S. 1964. The American oyster Crassostrea virginica (Gmelin), U.S. Fish Wildlf. Serv. Fish. Bull., 64, 1–480. Grave, C. 1905. Investigations for the promotion of the oyster industry of North Carolina, Rep. U.S. Fish Comm., 1903, 247–341. Harger, J.R.E. 1971. The effect of wave impact on some aspects of the biology of sea mussels, Veliger, 12, 401–414.





Hawkins, A.J.S. and Bayne, B.L. 1992. Physiological interrelations, and the regulation of production, in Gosling, E., Ed., The Mussel Mytilus: Ecology, Physiology, Genetics and Culture, Elsevier, Amsterdam, 171–222. Kauffman, E.G. 1971. Form, function, and evolution, in Moore, R.C., Ed., Treatise on Invertebrate Paleontology, Part N, Mollusca 6, Bivalvia, Geological Society of America, Lawrence, KS, N129–N210. Keck, R., Maurer, D., and Watling, L. 1973. Tidal stream development and its effect on the distribution of the American oyster, Hydrobiology, 42, 369–379. Khlebovich, V.V. 1969. Aspects of animal evolution related to critical salinity and internal state, Mar. Biol., 2, 338–345. Kinne, O. 1964. The effects of temperature and salinity on marine and brackish water animals, II. Salinity and temperature salinity combinations, Annu. Rev. Oceanogr. Mar. Biol., 2, 281–339. Kuenzler, E.J. 1961. Structure and energy flow of a mussel population in a Georgia salt marsh, Limnol. Oceanogr., 6, 191–204. Lawrence, D.R. 1971. Shell orientation in recent and fossil oyster communities from the Carolinas, J. Paleontol., 45, 347–349. Leigh, E.G., Paine, R.T., Quinn, J.F., and Suchanek, T.H. 1987. Wave energy and intertidal productivity, Proc. Natl. Acad. Sci. U.S.A., 84, 1314–1318. Liebig, J. 1847. Chemistry in Its Applications to Agriculture and Physiology, Taylor and Wilson, London, 240 pp. Lough, R.G. 1974. A reevaluation of the combined effects of temperature and salinity on survival and growth of bivalve larvae using response surface techniques, Fish. Bull., 73, 86–94. Monismith, S.G., Koseff, J.R., Thompson, J.K., O’Riordan, C.A., and Nepf, H.M. 1980. A study of model bivalve siphonal currents, Limnol. Oceanogr., 35, 680–696. Morton, B. 1980. Swimming in Amusium pleuronectes, J. Zool. Lond., 190, 375–404. Newell, C.R. 1990. The effects of mussel (Mytilus edulis) position in seeded bottom patches on growth at subtidal lease sites in Maine, J. Shellfish Res., 9, 113–118. Odum, E.P. 1983. Basic Ecology, Saunders, Philadelphia, 613 pp. Odum, E.P., Finn, J.T., and Franz, E.H. 1979. Perturbation theory and the subsidy-stress gradient, Bioscience, 29, 349–352. Peterson, C.H. 1991. Intertidal zonation of marine invertebrates in sand and mud, Am. Sci., 79, 236–249. Remane, A. and Schlieper, C. 1971, Biology of Brackish Water, Wiley-Interscience, New York, 372 pp. Rhoads, D.C. and Young, D.K. 1970. The influence of deposit- feeding organisms on sediment stability and community trophic structure, J. Mar. Res., 28, 150–178. Shelford, V. 1913. Animal Communities in Temperate America, University of Chicago Press, Chicago, 368 pp. Shumway, S.E. and Koehn, R.K. 1982. Oxygen consumption in the American oyster Crassostrea virginica, Mar. Ecol. Prog. Ser., 9, 59–68. Vernberg, F.J. and Vernberg, W B. 1972. Environmental Physiology of Marine Animals, Springer-Verlag, New York, 346 pp. Vincent, B., Desrosiers, G., and Gratton, Y. 1988. Orientation of the infaunal bivalve Mya arenaria L. in relation to local current direction on a tidal flat, J. Exp. Mar. Biol. Ecol., 124, 205–214. Vogle, S. 1981. Life in Moving Fluids: The Physical Biology of Flow, Willard Grant Press, Boston, 352 pp.





Wells, H.W. 1961. The fauna of oyster beds, with special reference to the salinity factor, Ecol. Monogr., 31, 239–266. Widdows, J. 1978. Combined effects of body size, food concentration and season on the physiology of Mytilus edulis, J. Mar. Biol. Assoc. U.K., 58, 109–124. Wildish, D.J. and Kristmanson, D.D. 1984. Importance to mussels of the benthic boundary layer, Can. J. Fish. Aquat. Sci., 41, 1618–1625. Wildish, D.J. and Kristmanson, D.D. 1993. Hydrodynamic control of bivalve filter feeders: a conceptual view, in Dame, R.F., Ed., Bivalve Filter Feeders in Coastal and Estuarine Ecosystem Processes, Springer-Verlag, Heidelburg, 299–324. Wildish, D.J., Kristmanson, D.D., Hoar, R.L., DeCoste, A.M., McCormick, S.D., and White, A.W. 1987. Giant scallop feeding and growth responses to flow, J. Exp. Mar. Biol. Ecol., 113, 207–220. Wildish, D.J., Kristmanson, D.D., and Saulnier, A.M. 1992. Interactive effect of velocity and seston concentration on giant scallop feeding inhibition, J. Exp. Mar. Biol. Ecol., 155, 161–168.





3

Organismic Level Processes

INTRODUCTION Organismic level processes, e.g., feeding, respiration, excretion, and growth, are often fundamental to examining the structural and functional roles of bivalves at the population and ecosystem levels. Traditionally, these organismic rate processes have been summed, equivalent to scaling up, to yield population and ecosystem estimates. Frequently these processes have been grouped together or integrated into ratios, either indices or budgets, in an effort to provide a deeper understanding of the underlying physiological or ecological processes. In a more ecological perspective, the energy or material budget (Bayne and Newell 1983; Crisp 1984; Griffiths and Griffiths 1987) has been utilized to further understand the various energy and material-processing relationships of organisms by summing a number of rate processes. The energy budget applies the laws of equilibrium thermodynamics to organisms and populations. Thus, it is assumed that for energy or material: Input = Output and that these terms can be expanded to: C=P+R+F+U Where C is the energy or material content of the food consumed; P is that quantity produced as tissues or gametes; R is that lost as metabolic heat or gas; F is the quantity lost as feces; and U is the amount lost from excreted urine and mucus. Production can be further divided: P = Pg + Pr Where Pg is the energy or material concentrated in new tissues and Pr that lost as reproductive material. Assimilation is defined as the amount of energy or material consumed (C) that is utilized by the organism. A can be calculated as: A = C – (F + U) = P + R The concept of “scope for growth” is defined as the difference between the energy of the food the animal consumes and all the other utilizations and losses (Warren and Davis 1967) and is readily derived from energy or material budgets. Such estimates have been applied to economically important bivalves including





Mytilus edulis (Widdows and Bayne 1971), Crassostrea virginica (Dame 1972), and Ostrea edulis (Buxton et al. 1981). These and other studies on bivalves indicate that the capacity of bivalves to regulate the various components of the energy budget by acclimation may enhance their ability to maintain a positive scope for growth. Results from such studies also suggest that outside the limits of acclimatory adjustment, energy balance considerations may limit the bivalve’s existence to a particular ecological niche (Buxton et al. 1981). In this chapter, bivalve physiological rate processes will be examined and related to various integrative measures, including budgets. This approach will develop an understanding of how estimates of ecosystem level rates are achieved through scaling up from organismic rate measurements.

FEEDING From an ecosystem perspective, feeding is the input of energy and materials into the bivalve. A number of quite different feeding mechanisms have evolved in the bivalves. Filter or suspension feeding is one mechanism that allows the bivalve to remove suspended microscopic particulate materials from the water column. Bivalve filter feeders pump or process water through a structural internal filter that usually retains particles irrespective of their food quality. Deposit feeding is typical of infaunal bivalves living in soft sediments. In this type of feeding, particles on the surface or within the substrate, i.e., deposits, rather than suspended sediments are collected by the bivalve and utilized as food. More specialized in their feeding mechanisms are boring bivalves and bivalves with symbiotic algae or bacteria in their tissues.

FILTER (SUSPENSION) FEEDING As noted earlier, bivalves evolved in shallow coastal seas where there was an abundance of suspended particulate material, usually dominated by phytoplankton. Because most bivalve filter feeders are sessile or semisessile as adults, these animals must pump and filter volumes of water considerably greater than that immediately adjacent to their habitat in order to consume sufficient phytoplankton to survive. The pumping and filtering mechanism used by bivalves has been a point of biological interest for a considerable time and an understanding of the structure and function of this mechanism is crucial to understanding the types of observations made and translated from the organismic level to the ecosystem level.

THE BIVALVE FILTER

AND

PUMP

The process of bivalve filter feeding is the result of the combined action of three types of cilia on the gill filaments (Figure 16). The lateral cilia are the main water movers and beat with a metachronal wave that assures a minimum distance between the cilia in order to maintain maximum water movement (Sleigh and Aiello 1972). As the water is moved or pumped through the gills, potential food particles are retained by the laterofrontal cirri in a number of ways. The particles may be sieved, © 1996 by CRC Press LLC




FIGURE 16. Water currents passing through the typical bivalve shell cavity, with a crosssectional view of a gill filament showing the different types of cilia.

intercepted, and impact with the gill through inertia, motile particle motion, or gravitational deposition. Except for sieving, all of these potential ways of particle interception allow for the trapping of particles smaller than the spaces between the cirri of the filter. In addition, particles are carried along in free suspension or caught up in mucus and transported by the frontal cilia in mucus trains or strings towards the labial palps and mouth (Jørgensen 1990; Ward et al. 1993). At the labial palps, particles are sorted either to be transported to the mouth or rejected as pseudofeces. Although I have presented the bivalve filter as a more mechanical device, Jørgensen (1990) has argued in a controversial fashion that it is a fluid mechanical filter where the complex patterns of laminar currents at the interfilament canals transfer particles across streamlines from through flowing currents to surface currents. Recent in situ observations using a fiber optic probe (endoscope) indicate that both mechanical and hydrodynamic filtration mechanisms appear to function in bivalves (Ward et al. 1993) and that these two mechanisms are not mutually exclusive. These authors also directly confirmed that mucus is important in the normal feeding of bivalves. In their study, Mytilus edulis used mucus strings on the ventral grooves of the gill filaments, Placopecten magellanicus mainly used a hydrodynamic slurry in the dorsal tracts, and Crassostrea virginica utilized both mechanisms (Ward et al. 1994). These workers speculate that the two mechanisms are efficient under different environmental conditions. The regulation of bivalve filtration rates has also been a contentious issue in recent years. One school of thought (Jørgensen et al. 1986; Jørgensen 1990) main© 1996 by CRC Press LLC




tains that the bivalve filter pump is basically controlled by the physical properties of the filter pump and the water that flows through the system. Jørgensen and his colleagues argue that variations in pumping rate in bivalves in response to temperature can be explained by changes in kinematic viscosity of the flowing water. They base this contention on the correlation between viscosity and filtration rate. Their views do not explain how the pump responds to environmental variation. The physiological school led by Bayne argues that body size, temperature, physiological condition, and suspended particulate material quantity and quality are important in explaining the variability of bivalve filtration rates. As the filtration rate shows an acute response to changes in temperature, and temperature is most likely a major and fundamental controlling factor on metabolism in poikilotherms (Kinne 1964), Willows (1992) suggests that a general explanation, based on temperature dependence of metabolism, is an underlying cause for filtration rate variability. This view is supported by many studies on the physiological acclimation of filtration rate to temperature (Widdows and Bayne 1971; Widdows 1976). As with temperature controls, the rapid and compensatory decline in filtration rate in response to increased particulate loading is also attributed to physiological processes (Widdows 1976). Thus, a physiological explanation of filtration rates in bivalves seems to be more persuasive at this time.

FILTRATION

AND

PARTICLE QUALITY

In natural ecosystems, filter feeding bivalves pump water containing a variety of particles of differing qualitative food values. It is common for suspended inorganic particles of little or no food value to be present in much higher concentrations than phytoplankton and other organic particles. The high concentrations of inorganic particles essentially reduce the food value of the total suspended particulate material. If bivalve filter feeders could qualitatively select particles they could offset the inorganic seston dilution effect. While some research (Winter 1978) asserts that filter feeding bivalves have no qualitative particle selection ability, other long-standing evidence from bivalve stomach contents shows that the particles in the gut are not in the same proportions as those in the adjacent water column (Grave 1916; Morse 1944). In a series of observations, Kiørboe and Møhlenberg (1981) showed that the efficiency of selection varied from almost nil to 15%, depending on species (Figure 17). The efficiency of selection was clearly related to palp size, but not gill type or turbidity in the respective bivalve’s environment. Additional studies by Shumway et al. (1985) concluded that not only are the palps selective, but the gills and stomach may also play a role in particle selection. Other work by Kiørboe et al. (1981) found that sorting did not commence until a minimum concentration or threshold value of suspended inorganic particulate material had been reached. This threshold appears to occur when the concentration of suspended matter exceeds the capacity for ingestion of material retained by the filter. It also appears to be the point at which mucus secretion increases and thus entangles particles to be ejected as pseudofeces (Jørgensen 1990). In Mytilus edulis, this threshold value was 1 mg/l of suspended material (Kiørboe et al. 1981). In the same vein, Newell and Langdon (in press) © 1996 by CRC Press LLC



8045_chapter 3_frame Page 45 Monday, January 20, 2003 2:46 PM

tems have become feasible. These systems allow longer time frame measurements, steady-state concentration of particles, and potential experimental manipulations; maintain oxygen concentrations; avoid metabolic waste build up; and can be adapted to field conditions. In these systems, filtration rate is computed as: FR =

[IN] - [OUT] ¥ x FLOW [IN]

where FR is the filtration rate, IN is the input particle concentration, OUT is the output particle concentration, and FLOW is the rate of water flow through the system. The animals in the chamber are actually filtering from a concentration that may be different from IN, particularly at low flow rates (Walne 1972; Bayne et al. 1976). Thus, sufficiently high flow rates should be chosen to avoid this problem, or the adjustment recommended by Hildreth and Crisp (1976) should be taken into account. This adjustment uses the concentration of particles in the immediate area of the bivalve in the denominator of the relationship instead of the input concentration. Although the preceding formulations provide estimates of filtration rate, the rates derived are difficult to scale up to populations or communities of organisms. This difficulty arises because bivalves filter at different rates depending on biotic variables, i.e., size, and physical variables, i.e., temperature. Size is most often modeled as an allometric relationship of the general power function: FR = aWb where W is the dry weight of the soft body and a and b are the intercept and exponent, respectively. The values for b usually vary between 0.67 and 1.00, indicating a proportionality between surface area and body weight (Winter 1978). As an alternative to weight, shell length is often substituted, but such linear measures are usually considered less accurate than weight measures (Dame 1972; Winter 1978). It should also be noted that models built from animals feeding on a single type of particle, monoculture of phytoplankton or inert suspended material, overestimate filtration when compared to models developed from bivalves feeding on a variety of suspended particles (Doering and Oviatt 1986). These authors offer the only example of combining temperature and size to estimate filtration rate. Their model is: FR = [(Lb1)(Tb2)]/a where L is length and T is temperature in °C. By adding temperature to their model, Doering and Oviatt (1986) increased the amount of variation explained by about 25%. In general, filtration rate decreases as suspended particle concentrations increase (see Winter 1978 for review). Such observations imply that bivalves regulate the amount of water from which particles are removed in relation to food concentration. Winter (1978) provides a schematic representation of the relationships between food concentration and filtration rate (Figure 18). In this scheme, as food concentration © 1996 by CRC Press LLC


FIGURE 18. A generalized representation of filtration rate and ingestion rate as a function of suspended cell concentration. (Redrawn after Winter 1978.)

rises from some threshold value, filtration rate increases rapidly and stays constant until a maximum of food is ingested. As soon as this maximum ingestion rate is reached, the filtration rate decreases continuously, while food ingestion remains constant. This pattern remains unchanged until the adequate food concentration is reached, after which pseudofeces production begins. At still higher food concentrations, however, filtration and ingestion rates are drastically reduced. These relationships will vary according to particle size, with smaller particles needing higher concentrations to be equivalent to larger particles. The ingestion rate of particles by bivalves is also a function of body size, temperature, and food concentration. As long as pseudofeces are not produced, the amount of food ingested is equal to the amount of food filtered (Winter 1978). This level of particle concentration is important in aquaculture and is known as the “pseudofeces-free cell density.” This concentration appears to be very close or equal to the optimum food concentration, because of the low energy demand for filtration and the high filtration efficiency of algal cells (Winter 1978). Recently, Willows (1992) developed a functional model of the feeding behavior and physiology of filter feeding bivalves. This model assumes that the net rate of energy gain from the available food sources is maximized. The model is different from previous empirical and physical models in that it optimizes for feeding mainly through physiological adaptation to variations in food quality.

DEPOSIT FEEDING Deposit feeding bivalves generally inhabit muddy low energy environments, while suspension feeders are more commonly associated with coarser sediments in more energetic environments dominated by tidal and wave-induced currents. Compared with filter feeding bivalves that pump large quantities of water and filter this water for small quantities of suspended particulate food, deposit feeding bivalves not only pump water, but also remove large quantities of deposited sediments from the © 1996 by CRC Press LLC


surrounding benthic environment in order to gain a relatively low percentage of quality organic material. Deposit feeding bivalves meet most of their nutritional needs from the organic portion of the sediments they ingest. Some bivalve deposit feeders can switch back and forth from suspension feeding to deposit feeding or feed in both modes simultaneously, depending on the conditions in their environment. Thus, the classification of a bivalve’s status as a deposit feeder may be relative. Bivalve deposit feeders use the same pumping mechanism as is used by bivalve filter feeders to move water through the animal. Unlike the surface-dwelling filter feeders, many, but not all, deposit feeding bivalves have lengthy incurrent and excurrent siphon tubes that insure the continuity of flow from the benthic–pelagic interface to the animal buried in relatively unconsolidated muddy sediments. For example, in the clam Scrobicularia, the inhalant siphon extends and moves across the sediment surface during low tide sucking up surface particles, but retracts during high tide to avoid predation by fish and crabs (Hughes 1969). In the more primitive bivalves, e.g., Nucula, Solemya, and Yoldia, there is little siphonal development and the animal moves through the muddy sediments ingesting sediments through the incurrent opening. For example, the file clam, Yoldia, uses its siphons for water flux, but not feeding. Instead, it uses two grooved tentacle-like appendages to feed. The cilia on these grooves move particles to the clam’s mouth (Levinton 1982). Because the food quality or organic content of sediments is very low, deposit feeding bivalves have developed two approaches to feeding: bulk feeding and sorting. In bulk feeding, large volumes of sediments are processed through the digestive tract in order to gain a small amount of nutrition. Bivalve deposit feeders typically sort particles before they are ingested into the mouth and reject the majority of the particles as pseudofeces (Lopez and Levinton 1987). While there are probably no completely nonselective deposit feeding bivalves, the process of sorting quality food particles from the great mass of poor quality particles results in a lower feeding rate and, in turn, a longer residence time for the food in the gut. As noted earlier for filter feeders, a longer gut residence time enables the digestion of the more refractory organic compounds common to the benthic environment. Thus, deposit feeding bivalves can process up to 20 times their body weight in sediments per hour with as much as 90% of these sediments egested as pseudofeces (Lopez and Levinton 1987). As deposit feeders feed on the sediments, a number of fundamental question arise. What are the sources of deposit feeding bivalve nutrition? Which components of the sediments are more important as food sources? In this mixture of particles, how does the bivalve separate quality food from poor food?

MICROBIAL STRIPPING Studies by Newell (1965) first touted the importance of microbes as food for deposit feeding bivalves. He concluded that Macoma balthica ingested both organic material and microbes, but only digested the microbes. This process is referred to as “microbial stripping.” Newell (1965) further suggested that the egested organic particles were recolonized by microbes after egestion, and these particles could again be



ingested and stripped of microbes, thus making the deposit feeder a major component of a decomposition feedback loop in the sediments.

CELLULASE ACTIVITY

AND

DETRITUS FEEDING

Although the microbial stripping idea focused on the microorganisms as food, it left unclear the role of organic matter as a food source. One approach to examining the role of organic matter as food for bivalve deposit feeders was to determine if the animals produced cellulase enzymes in their gut. In a survey of bivalve species, Crosby and Reid (1971) found that in both suspension feeding and deposit feeding bivalves, cellulytic activity generally corresponds to the level of cellulose in the food. In the typically deposit feeding genera investigated, Yoldia and Macoma, cellulytic activity was comparatively low. Crosby and Reid (1971) suggested suspension feeding bivalves have higher cellulase activities than deposit feeders because suspended food includes dinoflagellates that have a cellulose cell wall. Thus, if cellulose is not a general food for deposit feeding bivalves, microbes must be.

PARTICLE SELECTION In deposit feeding bivalves, the initial selection of particles occurs with the location and movement of the incurrent siphon or with palp tentacles. Yoldia, for example, can use its tentacles to reject up to 95% of the sediment collected (Bender and Davis 1984). As with suspension feeding bivalves, deposit feeding bivalves can also use the size of their filter to select particles. Both tentacles and filters appear to select for finer particles rather than larger particles and this process favors increased particle surface area and microbes. In addition to these selective mechanisms, many tellinid bivalves, e.g., Macoma and Scrobicularia, have complex stomachs capable of sorting and retaining smaller and less dense particles as opposed to larger particles (Hylleberg and Gallucci 1975). Some of these bivalves may also be adapted for stripping microbes from the ingested particles (Lopez and Levinton 1987). Finally, in some deposit feeding bivalves, the bacteria in the stomach are able to alter the composition of the organic matter in the stomach. This observation led Hylleberg and Gallucci (1975) to suggest that in Macoma nasuta the stomach may be compared to a chemostat, where dilution rate and multiplication rate of bacteria are balanced, yielding a net nutrition gain to the bivalve.

PROPORTION

OF

FOODS

Like strictly suspension feeding bivalves, deposit feeding bivalves remove phytoplankton, microzooplankton, organic and inorganic particles, and microbes, including bacteria, fungi, and microalgae from the sediments and surrounding waters. They also probably absorb dissolved organic materials in much the same manner as their filter feeding relatives. The determination of the relative proportions of the various food sources for deposit feeding bivalves is a major problem (Lopez and Levinton 1987). Some success has been found in combining the 14C-formaldehyde technique of Lopez and Crenshaw (1982) with the 14C:31Cr method of Callow and Fletcher (1972) to estimate © 1996 by CRC Press LLC




the absorption of organic materials. As each of the major food resources for deposit feeding bivalves has a different stable isotope ratio, the use of multiple stable isotope analysis to determine sources of materials and trophic status may also have utility in these endeavors (Peterson et al. 1985).

OPTIMAL FORAGING FOR FOOD IN THE SEDIMENTS The concept of optimal foraging is probably so important to the survival of bivalves that extant forms may be living close to their preferred optima (Hughes 1980). As bivalve deposit feeders are not very motile, their foraging strategies are mainly a function of ingestive and digestive processes (Taghon and Jumars 1984). Thus, foraging models (Figure 19) for these organisms stress ingestion and time dependent absorptions of food (Lopez and Levinton 1987). Because of the fine particle nature of the sediments, particle selection is better modeled stochastically (Jumars et al. 1982) and the range of food value is broad, varying from bacteria and digestible plant debris to undigestible materials. As microbial organisms and organic matter are inversely correlated with sediment grain sizes (Yamamoto and Lopez 1985), it is expected that a model of optimal ingestion will predict selection for fine particles (Taghon and Jumars 1984). Microbial feeding with the concurrent production of feces (fecal pellets) may actually stimulate microbial growth through maintenance of logarithmic growth of the microbe populations via grazing and by enriching the sediments with nutrients as they pass through the gut. As a bivalve increases its feeding rate, more food reaches the gut, but gut passage time and digestion rate decrease. This balance of digestion and food reaching the gut sets up an optimal feeding rate that should increase with increasing food quality. Alternatively, Calow (1975) has argued that as food quality decreases, gut residence time should increase to allow increased digestion. Although these strategies seem at odds with each other, if the gut length is longer for bivalves feeding on poorer quality foods, then the ingestion rate need not change. This latter strategy is observed in deep sea bivalves (Allen and Sanders 1966).

SHIPWORMS Several families of bivalves are specialized for burrowing or tunneling into hard substrates. Species in the genera Bankia, Lyrodus, Martesia, and Teredo are specialists at boring into wood and are commonly called shipworms. Because these bivalves eventually destroy their habitat, they have developed a number of adaptations that enhance their success in their transient environment. These include: (1) a shell that is an effective rasping tool; (2) a fast growth rate to take advantage of the transient nature of their habitat; (3) early maturation of gonads; (4) high fecundity; (5) incubation of larvae; (6) protandry; and (7) enzymes for cellulose breakdown (Morton 1978). While all shipworms maintain their ability to filter feed, it is the development of what appears to be a step-wise process of utilizing cellulose derived from wood that has allowed these bivalves to exploit their special habitat in the marine environment. First the shell rasps a tunnel into a piece of wood; then the wood particles are taken into the mantle cavity and through a selective sorting mechanism the small fragments are swallowed; in the esophagus, the organ of Deshayes with its symbiotic © 1996 by CRC Press LLC




FIGURE 19. The hypothetical relationships between optimal ingestion rate, increasing ingestion, decreasing digestion, and food quality in deposit feeding bivalves. (Redrawn after Lopez and Levinton 1987.)

bacteria secretes cellulytic enzymes; in the Teredinidae, the stomach further sorts the wood particles and additional cellulytic enzymes are produced; finally, the products of lignocellulose decomposition are absorbed by the digestive diverticula and digestion continues intracellularly. Thus, as is typical of other bivalves, digestion is a two-step process with an extracellular digestive sequence and an intracellular sequence (Morton 1978). Although a similar mucous-producing organ is found in other molluscs, the organ of Deshayes is unique to the shipworm bivalves. It not only produces digestive enzymes that aid in the processing of cellulose, but it may be the only case to date in the animal kingdom of nitrogen fixing bacteria in pure culture in a particular organ (Waterbury et al. 1983). In summary, shipworm bivalves can play a major part in the decomposition of woody materials in the sea. During the process of adaptation to this role, they may have developed a truly unique symbiotic relationship with nitrogen fixing bacteria.

SYMBIOTIC NUTRITION There are two fundamentally different types of autotrophic symbioses between bivalves and microbes. In one type, the relationship is between a small number of tropical bivalve species found in coral reef environments and the dinoflagellates, Symbiodinium (=Gymnodinium) microadriaticum, also known as zooxanthellae. © 1996 by CRC Press LLC




These autotrophic symbioses are driven by solar energy mediated by photosynthesis (Yonge 1936). The second type of symbiosis is between a variety of bivalves and bacteria living in the bivalves’ tissues. In these chemoautotrophic relationships, the bacteria are chemotrophic, obtaining energy from chemical sources; lithotrophic, because their energy source is inorganic; and autotrophic, because their source of cellular carbon is inorganic (Fisher 1990). As some of these bacteria utilize methane as an energy source and because their cellular carbon source can be organic, these forms are called methanotrophic. While the first bivalves exhibiting chemotrophic symbioses were found around deep sea hydrothermal vents, a great variety of bivalves from mainly anaerobic sulfide-rich environments have now been observed to exhibit chemoautotrophic and methanotrophic symbioses.

PHOTOAUTOTROPHIC SYMBIOSES Members of the tropical giant clam family, Tridacnidae (Tridacna gigas, T. maxima, T. derasa, T. squamosa, T. crocea, Hippopus hippopus and H. porcellanus) as well as the heart cockle, Corculum cardissa, have symbiotic relationships with the zooxanthellae. Almost all of these bivalves are associated with coral reefs where the same species of zooxanthellae is symbiotic with many massive reef building (hermatypic) corals. As with the massive deposition of coral matrices composed of calcium carbonate, the bivalves containing zooxanthellae have a tendency to massive calcium carbonate shells. One species, T. gigas, is known as the giant clam and has been reported to exceed 1.2 m in length and 250 kg in weight (Yonge 1936), making it the largest living bivalve. Only certain extinct species of rudist exceed the tridacnids in size, and they also may have had symbiotic zooxanthellae in their tropical/coral reef habitat (Kauffman and Sohl 1974). Early observations on these large coral reef bivalves quickly focused on the absence of sufficient planktonic food to support their metabolism (Yonge 1936). Furthermore, these bivalves appeared to absorb dissolved inorganic compounds. Various microscopic studies showed that unicellular zooxanthellae were living in the hemal sinuses of the hypertrophied siphon of these bivalves or what is commonly referred to as the “mantle tissue” in tridacnids (Yonge 1936) and to a lesser extent in the other organs (Goreau et al. 1973). Unlike corals where zooxanthellae are within the cells of the corals, these algae are found intercellularly in the bivalves, which means the larval bivalves must be infected by the zooxanthellae for the symbioses to take place. This uptake of zooxanthellae from the environment apparently occurs in the veliger stage of the clam’s development (Fitt and Trench 1981). When submerged, tridacnid clams gape and extrude their mantle folds. This action exposes the zooxanthellae in these tissues to sunlight and permits photosynthesis to take place in the zooxanthellae. Although the clams may receive some nutrition from digesting zooxanthellae, most of the metabolic gain from the symbiosis is believed to be derived from released photosynthates (Goreau et al. 1973, Trench et al. 1981), specifically glycerol and alanine (Muscatine 1967).





Both the zooxanthellae and the bivalve benefit from their relationship. The algae are sheltered, nourished with dissolved inorganic nutrients, and exposed to sunlight by their host. In turn, the clam has a ready source of inorganic and organic nutrients that are usually in low concentration in reef waters (Yonge 1936). Further, the uptake kinetics of inorganic compounds by this symbiosis seems to provide the capacity to take immediate advantage of spikes or surges in limiting nutrients, e.g., ammonium, much the same as has been shown in corals (Wilkerson and Trench 1986). The bivalve host can rapidly incorporate carbohydrates produced by the zooxanthellae into its metabolic processes (Goreau et al. 1973). However, these carbohydrates are not a source of nitrogen (zooxanthellae are carbon fixers, not nitrogen fixers) and protein to the bivalve. To gain these food components, the bivalve must filter phytoplankton and microzooplankton from the surrounding water. This dependence on normal sources of bivalve nutrition in the tridacnids is evidenced by the presence of feeding gills, selective palps, and an elaborate digestive system (Yonge 1975). There are numerous observations of tridacnids kept in the dark with and without plankton. These experiments usually result in a loss of zooxanthellae and, if plankton is present, survival of the host. Because of the symbiosis exhibited between zooxanthellae and tridacnid clams, a number of studies have focused on the role of the zooxanthellae in the bivalve host’s nutrition. These studies have been limited to examining if and how nutrients are passed from the zooxanthellae to the bivalve, the role of light in controlling photosynthesis by the zooxanthellae, and determination of the production:respiration (P:R) ratio. Early studies (see Goreau et al. 1973 and Fankboner and Reid 1990 for reviews) contended that zooxanthellae were captured by amebocytic blood cells, with digestion occurring in the blood stream and indigestible products being removed by the kidneys. Light and electron microscope studies by Trench et al. (1981) found no evidence for zooxanthellae in blood amebocytes. These authors also found no support for tridacnids digesting their symbionts and the undigested components collecting in the kidneys. In fact, the deposits in the kidneys were found to be mineral phosphorus. Using radioactively labeled carbon dioxide (14CO2), Goreau et al. (1973) were able to clearly show that uptake of label by the zooxanthellae and the eventual transmission of the labeled products via the blood to the rest of the bivalve. Thus, it appears that it is the photosynthetic products of the zooxanthellae that are utilized for food instead of the zooxanthellae themselves. Tridacnids expose their zooxanthellae-containing mantle tissues only during the day and are nocturnally inactive (Reid et al. 1984). This observation also focuses on the importance of the zooxanthellae symbionts as a source of nutrition, because the great majority of plankton in coral reef waters is usually only over the reef during night, while the zooxanthellae require exposure to light. Light plays a major role in the nutrition of tridacnid bivalves because of the light-limited nature of zooxanthellae. In essence, we must look at these clams as if they are primary producers rather than herbivores. Studies of oxygen uptake and release in Tridacna maxima (Trench et al. 1981) show that these bivalves are adapted to strong light intensities typical of shallow coral reef environments and show no signs of photoinhibition. By comparing light-driven evolution of oxygen (production © 1996 by CRC Press LLC




+ respiration = net production) to dark uptake of oxygen (respiration), Fisher et al. (1985) clearly showed P:R ratios greater than 1.0. At lower light intensities, smaller clams have higher P:R ratios, probably because more of their zooxanthellae are exposed to higher light intensities, while in larger clams, the thicker shells and bodies shade a sizable proportion of the zooxanthellae. Trench et al. (1981) estimated the relative contribution of zooxanthellae photosynthesis to respiratory carbon demand by the clam T. maxima. They utilized direct observations of respiration, net photosynthesis, and the proportion of net carbon translocated from zooxanthellae to the clam following Porter’s model (1980):

%C =

[(P

net

(

)

]

clam, 12 hday) .375PQ-- 1 + ( Rclam, 12 hnight ) (.375RQ) (95%) ( 40%)

(Rclam, 12 hnight ) (.375RQ) (2) (95%)

where %C is carbon assimilated, P is production, PQ is photosynthetic quotient, R is respiration, and RQ is respiration quotient. From this model that only requires oxygen concentration observations, estimates of zooxanthellae contribution to clam respiratory carbon needs on sunny days were 77 to 84% and on cloudy days 62 to 63%. Thus, the photosynthetic carbon produced by the zooxanthellae may provide over half of the respiratory carbon requirements of these tridacnid clams. These authors stress, however, that due to the many assumptions made in the models, these estimates should not be considered definitive. In more recent studies, Klumpp et al. (1992) and Hawkins and Klumpp (1995) found that giant clams deposit proportionally more carbon into their tissues relative to that respired than completely heterotrophic bivalves. Furthermore, small clams depended more on filter feeding (65%) for carbon needs, while large clams only acquire 34% of their carbon from this source — all of which supports the notion that with the development of clams from settlement to adult the symbionts also develop and become a major component in the clam’s nutrition. Another aspect of nutrition in this photoautotrophic symbiosis is that of the source and recycling of inorganic nutrients. In a series of studies, Fitt et al. (1993) and Belda et al. (1993) determined that nonsymbiotic larvae and young clams with few zooxanthellae release ammonium while large clams deplete ammonium and nitrate from sea water. Clams grown in elevated concentration of ammonium and phosphate showed an increase in the concentration of these elements in tissues of both the clam and the algae. Stoichiometric analysis revealed that the clams probably regulate the availability of phosphorus to the zooxanthellae. Using 15N-ammonium, Hawkins and Klumpp (1995) found there was a net uptake of ammonium from sea water which was modulated by nutritional history, light history, ammonium concentration, and possible biological rhythmicity. Zooxanthellae also assimilated nitrogen excreted by host tissues. Most of the nitrogen released by the zooxanthellae was incorporated into the host tissues with no significant loss from the clam. They concluded that the photoautotrophic symbiosis of the giant clam confers a nutritional advantage over nonsymbiotic bivalves because this symbiotic relationship tightly recycles limiting nutrients in a nutrient poor environment. © 1996 by CRC Press LLC


Thus, tridacnid clams are nutritional opportunists in a nutrient-poor environment. They filter feed on suspended particles including diatoms, crustaceans, and zooxanthellae released from heat-stressed corals; take up dissolved organic matter; and incorporate photosynthates released by the zooxanthellae (Fankboner and Reid 1990). In doing so, they reflect essentially the same nutritional diversity as the dominant corals in their ecosystem.

CHEMOAUTOTROPHIC SYMBIOSES Chemoautotrophic symbioses are widespread in marine bivalve molluscs (Fisher 1990). Both chemoautotrophic or methanotrophic symbionts have been clearly demonstrated in numerous species of bivalves (Table 2). While the behavioral, physiological, and morphological adaptations to their symbionts vary among the different families of bivalves, there are many similarities. Unlike the photoautotrophic symbionts, most of the chemoautotrophic symbionts are intracellular, with the Thyasiridae an exception. The various bacterial symbionts appear to be associated with bacteriocytic cells and are often located in cellular vacuoles. These associations are found in a wide range of habitats, usually at the interface between aerobic and anaerobic environments. The successful bivalve symbioses appear to bridge this interface with numerous and often unique adaptations. As the chemoautotrophic symbionts are relatively small (prokaryotic in size), a variety of methods have been used to demonstrate their existence. These approaches include electron microscopical identification, level of enzymatic activity, presence of lipopolysaccharide, stable isotopic ratios, presence of elemental sulfur, unique physiological adaptations, and the anatomy and habitat of the host (Fisher 1990). Enzymatic studies focus on the presence and activity of specific enzyme systems responsible for chemosynthesis. The enzymes of interest are: 1. Ribulose-1,5-bisphosphate carboxylase-oxygenase (RuBPC/O) catalyzes the first reaction in the Calvin Benson Cycle; 2. Adenosine-5′-phosphosulfate reductase (APS reductase) catalyzes the reaction of AMP and sulfite; 3. ATP sulfurylase catalyzes the reversible reaction of adenosine-phosphosulfate and pyrophosphate to yield ATP and sulfate; 4. Sulfate adenylyl transferase, in the same reaction as ATP sulfurylase, yields ADP instead; 5. Rhodanase catalyzes the splitting of thiosulfate into sulfite and sulfur; 6. Sulfide oxidase catalyzes the first step in the oxidation of hydrogen sulfide; 7. Nitrate reductase catalyzes the reduction of nitrate to nitrite; 8. Nitrate reductase catalyzes the reduction of nitrite to ammonia (see Fisher [1990] for a more detailed discussion). Another group of tools in the ecologist’s arsenal for identifying chemoautotrophic symbioses is the stable isotope ratios of carbon, nitrogen, and sulfur. Long





TABLE 2 Bivalves with Chemoautotrophic Symbionts Visual EM

Species Lucinidae Anodontia philippiana Codakia costata Codakia orbicularis Codakia orbiculata Linga pennsylvanica Loripes lucinalis Lucina nassula Lucina radians Lucinella divaricata Lucinoma aequizonata Lucinoma annulata Lucinoma atlantis Lucinoma borealis Myrtea spinifera Parvilucina multilineata Parvilucina tenuisculpta Pseudomiltha floridana Solemyidae Solemya reidi Solemya velesiana Solemya velum Thyasiridae Thyasira equalis Thyasira flexuosa Thyasira gouldi Thyasira sarsi Vesicomyidae Calyptogena elongata Calyptogena laubieri Calyptogena magnifica Calyptogena phaeseoliformis Calyptogena ponderosa Vesicomya cordata Vesicomya gigas Mytilidae Bathymodiolus thermophilus

+ +

+

+ + +

Enzymes

Ru Ru Ru, As, R Ru Ru Ru, Ar, As Ru Ru Ru, Ar, As Ru, As, R

δ

C(%)

–23.2 to –28.3

–23.0

+ –31.2 to –33.0 –24.1 to –29 –23.1 to –24.2

+ + + + +

Ru, Ar Ru, Ar, As Ru Ru, As Ru, Ar

+ + +

Ru, As, Ar, R

–30

Ru

–30.9 to –33.9

+ + + +

Ru Ru, Ar, As Ru, Ar, As

+ + + + + + +

Ru, As Ru, As

+

Ru, As

Ru, As

°S

+ + + +

–29.3 –32 –28.2 to –31

–32.1 to –51.6 –37.8 to –40.1 –31.2 to –39.1 –39.8

+

+ + + + + + +

–30.5 to –37.1

Note: Ar = APS reductase, As = ATP sulfurylase, R = ribulose 5′ kinase, Ru = ribulose bisphosphate carboxylase/oxygenase, °S = elemental sulfur in gills. From Fisher 1990.





known for their utility in determining the food source and web structure of ecological systems, these isotopic ratios are also useful in identifying chemoautotrophic symbioses. The sources of carbon, nitrogen, and sulfur elements for the various energygenerating reactions are quite different from those in nonsymbiotic bivalves. While the individual isotopic ratios of carbon (δ13C), nitrogen (δ15N), and sulfur (d34S) can give evidence for food sources, and carbon and nitrogen isotopes can reflect trophic level, it is the broad range and use of multiple isotopic ratios that provides the most useful information both in symbiotic studies as well as in ecosystem level analyses. Because elemental sulfur may serve as an energy storage product, a result from sulfide detoxification or as a by-product of sulfide oxidation, its presence in conjunction with other characteristics is a good indicator of chemoautotrophic symbioses. Although elemental sulfur is a good indicator, its presence is variable and is dependent on the physiological state of the symbiont (Fisher 1990). The anatomy of the host, particularly its feeding structures, often suggests the availability of some type of nutritive symbioses. In bivalves, these characteristics include lack of a gut, hypertrophied gills, and reduced particulate feed ability. Also, if the host bivalve is limited to habitats where the substrates necessary for chemoautotrophiy are present, then chemoautotrophy might be suspected (Fisher 1990). All hosts for chemoautotrophic symbionts must provide their symbionts with an electron donor, an electron acceptor, and a carbon source. The electron donor is usually some form of reduced sulfur, either hydrogen sulfide or thiosulfate, the electron acceptor is oxygen, and the carbon source is carbon dioxide or bicarbonate. As bivalves primarily utilize aerobic metabolic pathways, and sulfide is toxic to most enzyme systems and disappears in the presence of oxygen, bivalves have developed complex mechanisms for providing their symbionts with both reduced sulfur and oxygen. The bivalve species that have been suggested to contain chemoautotrophic symbionts and the evidence supporting these identifications are given in Table 2. In all species identified thus far, the symbionts are located in the gills and are intracellular in all but the Thyasiridae. All members of the family Lucinidae that have been examined contain symbionts (Fisher 1990). These bivalves typically have a reduced gut, reduced labial palps, no incurrent siphon, and large fleshy gills (Allen 1958). The Lucinidae are thought to obtain sulfide from the reduced sediments surrounding their burrows and oxygen from the overlaying water. Of the several chemoautotrophic species in the Mytilidae, Bathymodiolus thermophilus, the deep sea hydrothermal vent mussel, is the best studied (Fisher 1990, Kenk and Wilson 1985). These mussels have been found in a wide range of environmental conditions in the area of the hydrothermal vents, and this distribution has been attributed to their ability to obtain nutrition from symbioses (Fisher 1990), filter feeding (Le Pennec and Prieur 1984) and dissolved organic material (FialaMedioni et al. 1986). Stable isotope ratios of mussels taken near the Rose Garden hydrothermal vent site on the Galapagos rift support the suggestion that multiple sources of nutrition are important to these animals (Fisher 1990). The family Solemyidae was initially an enigma to science because it is composed of relatively large prosobranch bivalves with reduced or absent digestive tract and feeding abilities (Reid 1980). All members of this family are now thought to contain © 1996 by CRC Press LLC



8045/chapter 3/frame Page 57 Tuesday, January 21, 2003 12:59 PM

chemoautotrophic symbionts. Further, these shallow water estuarine clams typically make deep burrows in organically rich sediments that penetrate both oxidized and reduced sediment layers. Dense populations of Solemya reidi are found in sites polluted from paper mill effluent and sewage sludge deposits that are high in reduced sulfides. Despite their symbiotic nature and their lack of a gut, these clams reach a size of up to 5 cm. The Thyasiridae are closely related to the Lucinidae, but they are notable in that their symbiotic bacteria are extracellular. The extracellular nature of the symbionts has been interpreted as indicating an early stage in the development of chemoautotrophic symbioses in this group compared to those groups with intracellular symbionts (Fisher 1990). Vesicomyids have been found in a variety of middepth to deep sea sulfidecontaining habitats, including hydrothermal vents, subduction zones, saline seeps, hydrocarbon seeps, and deep sea reducing sediments. Some species of these clams may burrow through the sediments, while others are epifaunal. The vent clam Calyptogena magnifica is one of the better studied of these chemoautotrophs. Here again, it is evident that the clam utilizes the interface between the oxidized and reduced environments to the best advantage of the symbiosis. These epifaunal clams of the hydrothermal vents orient their bodies such that the foot is exposed to warm reducing vent waters rich in hydrogen sulfide, while cooler overlaying water high in oxygen is pumped through the clam. Thus, a small number of bacterial species have succeeded in forming an endosymbiotic relationship with marine bivalves. As the bacteria are mainly sulfide oxidizers, these microbes benefit from the dependable interface (Reid and Brand 1986) the bivalve provides between the aerobic sediment surface and water column and the anaerobic environments of reducing sediments and hydrothermal vent environments. The bivalves benefit from an additional source of food or energy, and this feature may allow them to exist in environments they might otherwise be unable to inhabit.

PRODUCTION (P) Production is defined as the accretion of somatic tissues and/or gametes and has been extensively studied in bivalves (Hawkins and Bayne 1992). Production includes not only material and energy stored as new tissues and represented as growth of the individual (Pg), but also material that goes into gametes (Pr). Hawkins and Bayne (1992) have stated that production is controlled by the interaction between endogenous processes that pertain to the organism and exogenous factors from the external environment. Exogenous influences include quality and quantity of food, temperature, and salinity, and have been discussed elsewhere in this text. The major endogenous factors are body size, physiological status, and genotype. These internal influences determine maximal capacity for production. Production Due to Growth (Pg) Growth is one of the most-used measures of an organism’s vitality in a given environment. In bivalves, the animal’s size is directly related to its age, and this © 1996 by CRC Press LLC


cumulative increase in biomass with respect to time is termed “absolute growth,” while the percentage increase in biomass per unit time is “relative growth” (Seed 1976). As growth represents changes in bivalve size, it is most often measured as shell length, weight, and volume. There may be complications in just measuring single shell parameters, as shell growth may be different from soft body growth due to environmental factors or variations in the reproductive cycle of the bivalve. It is the soft body that carries out the living processes of the animal, not the shell. Thus, allometric relationships are often developed between shell parameters and body weight in order to nondestructively estimate soft body biomass on living bivalves (Dame 1972). Growth measurement Some methods used to assess growth in bivalves are following size changes in marked individuals, tracking size frequency distributions, measuring shell growth rings in relation to biomass, and observing radioactive tracer uptake. To determine seasonal growth rates as well as the influence of size and local environmental conditions, marked bivalves are often kept in wire cages at a particular depth or intertidal elevation. The cages partially protect the bivalve from predation and make them easier to retrieve than individual animals. Generally, cages do not influence growth, but Harger (1970) found that mussels kept in intertidal cages grew faster than those not in cages, possibly because wave action was reduced within the cages. Following a particular cohort by measuring size frequency distribution through time is a common technique among population ecologists (see Chapter 4). In this method, a given year class is followed, and the change in the average size of the mode is equivalent to average growth. This method only works well in bivalve species with a very narrow reproductive or recruitment period (Craig and Oertel 1966). If the recruitment period is extended, i.e., Crassostrea virginica (Dame 1972), or growth rates are variable, i.e., Mytilus (Seed 1976), then the method has limited application. Shell rings or growth lines are defined as abrupt or repetitive changes in the character of accreting bivalve tissue (Dillon and Clark 1980) and, depending on the circumstances, may be a post mortum indicator of growth. These lines are evident in some bivalves when they experience well-defined seasonal conditions, particularly suspended periods of shell growth (Seed 1976). Such periods are usually associated with extremes of temperature, wave action, or reproductive periods. Bivalves from environments with uniform conditions generally do not exhibit rings, and line formation is variable both between habitats and with a habitat. Thus, care should be taken to check the reliability of rings in each locality. Shell growth Growth of shell is quite different from growth of somatic and reproductive tissues. The bivalve shell is composed of both an organic matrix and crystals of calcium carbonate (CaCO3). There are three major aspects of shell growth and formation: (1) the role of metabolism in CaCO3 formation and the synthesis of the organic



matrix; (2) secretion of shell components by the mantle; and (3) CaCO3 crystal growth (Wilbur 1964; Wilbur and Saleuddin 1983). As CaCO3 and CO2 are both components of the calcium carbonate–carbon dioxide buffer system so prevalent in sea water, changes in the concentrations of any component in this buffer system influence the amount of the other components. 2+ + 2+ - CO2 + H2O fg H2CO3 fg HCO gCa 3 + H fgCO3 + H fgCaCO3f

alkaline g æ Ææ

¨æ

f acid

Increasingly alkaline conditions will drive this buffer system to the right with an increase in CaCO3, assuming sufficient calcium ions are present, and increasing acidity will drive the system to the left with the dissolving of CaCO3 and eventual production of CO2. The CO2 concentration within the bivalve’s tissues can also be a function of intermediary metabolism, and combined with the buffer system, potentially controls shell crystal formation (Wilbur 1964). The amount of calcium deposited in shell is also a function of the calcium concentration in the surrounding water and time of submergence. Early studies of intertidal bivalves clearly supported the above processes in that the longer the animal is submerged the greater the calcium uptake and consequently shell growth is higher (Rao 1953; Baird and Drinnan 1956). The organic matrix is secreted in insoluble form by the mantle and deposited as a layer on the inner shell surface. The matrix is proteinaceous and is the substrate upon which CaCO3 crystals initiate and grow. While measuring shell growth by weight in water (Havinga 1928; Andrews 1961) or by linear measures is straightforward, determining the organic matrix component of the shell, a relatively small component of growth, as a percentage of total weight is difficult. Although small in mass, in terms of calories or organic carbon, the organic matrix may be an important component of growth. The two most common ways of estimating the biomass of the organic matrix are through careful ashing in a furnace or acid dissolution of shell and weighing the remaining dried organic material (Dame 1972; Price et al. 1970). In addition to seasonal and reproductive shell growth rings that are visually external, microscopic growth increments or lines ranging from 1 to 100 m m thick are discernible within bivalve shells (Rhoads and Pannella 1970; Lutz and Rhoads 1980). These deposition increments are laid down during each 24-hour period of physiological activity (House and Farrow 1968; Clark 1968; Clark 1974). It is generally accepted that many, if not all, microgrowth increments in bivalve shells are a reflection of variations in the relative proportions of organic material and calcium carbonate (Lutz and Rhoads 1980). In many bivalves, these growth lines appear to be correlated with the tides and the fact that the valves are open during submergence and closed during exposure. To explain these lines, Lutz and Rhoads (1977) proposed that differences in organic concentrations in the various regions of the shell were simply residues left behind as a result of dissolution of shell material during periods of anaerobiosis. Subsequent studies have supported their hypothesis



(Gordon and Carriker 1978; Lutz and Rhoads 1980). Microgrowth increments have been documented in five temporal categories: (1) semidiurnal and diurnal, (2) fortnightly, (3) monthly, (4) annual, and (5) semiperiodic or random events (Lutz and Rhoads 1980). These microscopic lines provide information about environmental and physiological conditions of individual animals from both current and past environments (Table 3). Thus, the bivalve shell may be considered a long-term continuous environmental recorder. TABLE 3 Physiological and Environmental Events Recorded in Molluscan Growth Patterns Events

Characteristics

Time and Place

Ecological Application

Circadian Rhythms Spawning

Dark and light shell layers

Daily

Physiology

Sudden depositional break

Variable by species and place

Winter

Gradual reduction in deposition rate Thickest daily increment

Shallow water at mid and high latitudes

Regular recurrent patterns with 15- to 30-d cycle Sudden depositional break with rapid recovery

Intertidal and shallow water Storm frequency

Reproductive period and duration Climate, latitude, and geography Climate, latitude, and geography Sea level change

Summer Tides Storms

Weather

From Rhoads and Pannella 1970.

To summarize, shell growth is a function of calcium availability in water and, therefore, of the amount of water pump across the bivalve’s tissues, the pH of the bivalve’s internal system, the intermediary metabolism of the animal, and the environmental temperature that controls the rates of most of these processes. Although shell size is related to soft body tissue mass, it is not a direct measure of body size, because some of the controlling factors are different. Production Due to Reproduction (Pr) In addition to the energy and materials bivalves allocate to shell and body growth, they place considerable amounts of production into gonadal tissues (Pr). These tissues develop into gametes that are lost from individual during spawning. Consequently, there is a cyclical storage and loss of reproductive products that is controlled by endogenous and exogenous factors. There are numerous methods used to estimate the amount of production allocated to reproduction. The amount of Pr can be directly estimated by inducing the bivalve to spawn in the laboratory and then counting or weighing the gametes released. © 1996 by CRC Press LLC




[ [

Indirectly, Pr can be estimated from allometric relationships relating weight loss due to spawning to body weight or shell size (Bayne and Worrall 1980) and by estimating the proportion of gonad lost from the proportion of spatfall in a given time period (Dame 1976). The proportion of production devoted to reproduction is low in young bivalves, but gradually increases to a dominant proportion in adults. In the largest mussels, reproductive tissues may account for more than 50% of the soft body weight, and Pr may be >90% of total production (P) (Seed and Suchanek 1992; Thompson 1979). Bivalves may “conservatively” utilize nutrient reserves to buffer gametogenesis from environmental changes (Hawkins et al. 1985). These reserves may come from somatic tissues. Generally, gametogenesis is “opportunistic,” being supported by feeding alone (Hawkins et al. 1985). The condition index for bivalves relates the proportion of the shell cavity that is occupied by soft body tissue. Such indices have been used to follow seasonal change in gross nutrient reserves or meat quality, as well as to monitor various pollutants (see Chapter 8) and diseases (Crosby and Gale 1990). In a comparison of various methods of determining the condition index, Crosby and Gale concluded that the gravimetric formulation

Condition Index =

[ È

dry soft tissue wt(g) ¥ u1000 ˘ internal shell cavity capacity (g) ˙˚ Î

]

has less measuring errors, lower coefficients of variation, is the easiest and fastest to use, and is most meaningful as an index of current bivalve nutritive status and recent stress. These investigators stress the need for further investigations into the seasonal and age-dependent relationships between tissue/shell components and gravimetric condition indices in order to gain new insights into bivalve energetics. Growth Models Numerous models have been developed to describe the growth of individual organisms. The most useful models are those in which the components and constants have biological meaning and a few of these will be reviewed here. The simplest formulation is the monomolecular model lt = Ly (l - ekt) where lt is the size at time t; L• is the maximum size; and k is a constant representing the rate at which maximum size is approached. In this model there is no inflection point, and growth rate declines linearly with increasing size. Maximum size can be determined from observed data or from a Walford plot (Walford 1946): l t = bL t +1 + a © 1996 by CRC Press LLC


Where this linear relationship intercepts the no-size-change line is an estimate of maximum size. This function is often used to represent the later portions of life (Richards 1959). The autocatalytic or logistic model lt =

Ly

( 1 −- e -

- kt )

produces a symmetrical or s-shaped curve about an inflection point. Its relative growth rate declines linearly with increasing size. This model has been used as a convenient empirical curve (Richards 1959). The Gompertz model lt = L y e - -e

-kt

or

[

log l t = log L y 1 - - e - - kt

]

resembles the logistic model, but is asymmetrical. Linear relations exist between its relative growth rate and log l and between log l and time. The von Bertalanffy model (Bertalanffy 1957): lt = Ly[ 1 - e -k ( t- t0 )]

in its general form includes all of the preceding models. This model has been favored by biologists because of this generality and its derivation from allometric and metabolic relationships with biological meaning (Figure 20). Several investigators (Taylor 1959, 1960; Ursin 1963) have adapted the von Bertalanffy model to temperature and bivalve growth. These investigators use the product of the number of days and the temperature for those days, day-degrees, to represent the environmental variable. The following is an elegant example of utilizing day-degrees to represent temperature influences on growth: lD = Ly [ l-e-kD (D-D0) ] where lD is length at D day-degrees, KD is the rate constant determined as k/Dy (Dy = annual sum of day-degrees) and D0 = t0 (see Bayne and Worrall [1980] for an example). The preceding models utilize size data to estimate growth. An alternative approach to estimating growth is based on the energy budget equation and generating © 1996 by CRC Press LLC


FIGURE 20. A generalized comparison of the Gompertz and Von Bertalanffy growth curves in bivalves.

an estimate of growth potential or scope for growth (Warren and Davis 1967; Bayne et al. 1976). When these observations are integrated over time and applied to individuals of different sizes, an average growth curve can be derived. Respiration (R) At the ecosystem level, respiration represents a measure of the energetic cost of supporting a given bivalve. Respiration is a unique component of the energy budget because it is entirely a loss term. The matter associated with respiration is recycled as CO 2 and water and energy is lost as waste heat to the environment. At the level of the organism, respiration represents all the work a bivalve must perform in order to survive. Finally, respiration is the most thoroughly and precisely measured process in the energy budget. Because of this, there is an extensive body of knowledge and theory explaining respiration. In bivalves, respiratory gas exchange between the water and the animal occurs primarily at the gill. The bivalve gill has a high surface area due to the folding of the tissues or demibranchs, and this feature increases the ability of the animal to exchange respiratory gases. The demibranchs are also well supplied with blood vessels and this characteristic ensures the rapid movement of gases into and out of the bivalve. Last, large volumes of water are pumped or moved by the cilia on the gill. This action provides a constant renewal of water within the bivalve so that fresh water with higher oxygen levels is constantly provided and stale waters with higher waste gas concentrations are constantly flushed from the animal. Thus, in addition © 1996 by CRC Press LLC




to being the main feeding organ of filter feeders, the gill is also the main respiratory organ. Aerobic respiration involves the utilization of organic carbon compounds as sources of matter and energy. In its most fundamental form: Organic-C + O2 → CO2 + H2O + Energy Estimates of metabolism usually focus on the measurement of changes in one of the components of the preceding relationship. In actuality, oxygen concentration is the most commonly measured estimator, although carbon dioxide and heat are also used. Once one component of the metabolic equation is known, the others can be calculated. If the organic carbon source is unknown or varying, then measurement of both oxygen and carbon dioxide allows the computation of the repiratory quotient (RQ) and thus an estimate of the type of carbon compounds being metabolized. Oxygen consumption is directly related to the size of the bivalve by the allometric power function: R = aWb where R is oxygen uptake, W is the body weight of the bivalve, a is the intercept, and b is the slope. Surveys of respiration-to-weight relationships for many different animals, including bivalves (Hemmingsen 1960) found that the coefficient b is about 0.75. In bivalves, estimates of b may vary from 0.5 to 1.0, but Bayne et al. (1976) note that deviations from b = 0.75 are often attributed to a narrow size range in the observed animals. Kruger (1960) recommends a size range of 1:50 from smallest to largest individuals to provide reliable estimates of a and b. Peters (1983) has made a number of points concerning the oxygen consumption to size relationship. First, the apparent constancy of the slope (b = 0.75) shows that the proportionality is unaffected by size. Second, the positive value of b means larger animals respire at higher rates than smaller individuals. Third, as b < 1 the metabolic rate rises more slowly than body size. Finally, the data are scattered, which suggests the relationship should not be interpreted as deterministic. As metabolism is the summed energetic cost of an organism’s life processes, the relationship between size and respiration should be reflected in other biological relationships. Thus, the power function, b = 3/4, is often successful in describing scaling for other rates. This parallelism is called the principle of similitude (Thompson 1961). Although the surface law and dimensional analysis are most often given as the explanation for this allometric relationship, each has its problems (see Peters 1983) and there is no consensus. Because most adult bivalves are relatively sessile in their benthic habitats, many of these animals are exposed to anaerobic as well as aerobic conditions. Hence, bivalves are defined as facultative anaerobes, i.e., they can live aerobically or anaerobically, but preferentially use oxygen for respiration because of its higher efficiency in producing energy during intermediary metabolism (Zwaan and Mathieu 1992). Anaerobic conditions can occur in bivalves when they seal their valves during © 1996 by CRC Press LLC




exposure at low tide or when their external environment has reduced oxygen concentration. In some cases, hydrothermal vents and some sediments, the bivalves live at the interface between aerobic and anaerobic environments and through the presence of symbiotic bacteria utilize inorganic compounds as energy sources. Some of these compounds, i.e., H2S, are effective poisons to aerobic respiration by inhibiting cytochrome function and blocking O2 uptake by hemoglobin. Anaerobic metabolism is a normal part of the production of energy by metazoans. However, energy production through anaerobic metabolism is somewhat lower than through aerobic metabolism. In adult bivalves lacking red blood cells, the animal can switch between aerobic and anaerobic metabolism, depending on oxygen concentrations in the environment (Mangum and Van Winkle 1973). There is an ecological advantage to switching to anaerobic metabolism. Anaerobic metabolism is reduced and this reduction lowers total metabolic activity and energy demand. In intertidal bivalves, feeding stops during low tide exposure; therefore, the carbon sources for metabolism are reduced and lower metabolism (anaerobic) is favored. Reduced metabolism and anaerobiosis during winter months are thought to be important factors in freezing temperature survival in Geukensia (Aarset 1982). In this case, anaerobic metabolism end products may act as antifreeze or cryoprotectant (Loomis et al. 1988). While the determination of aerobic respiration through oxygen uptake is well known and developed, determination of anaerobic metabolism and total metabolism (aerobic + anaerobic) are less so. Anaerobic metabolism is often estimated indirectly by measuring anaerobic metabolic endproducts. Total metabolism (Figure 21) can be estimated by summing aerobic and anaerobic estimates or by directly measuring total heat production with a calorimeter (Shick et al. 1983). The heat production method was first used on invertebrates by Gnaiger (1977) and later applied to aerobic bivalves by Hammen (1979) and anaerobic bivalves by Hammen (1980) and Pamatmat (1979). The indirect approach to estimating anaerobic metabolism from endproducts in bivalves was led by Zwaan (1977) and others. Originally, it was thought that the direct production method produced a greater estimate of metabolism than could be accounted for by endproducts (Gnaiger 1980). However, later studies (Shick et al. 1983) showed that individual organism variability was large enough to explain the discrepancy. Thus, the indirect and direct methods of determining metabolism are comparable. As noted earlier, oxygen consumption increases with bivalve size according to the power law (b = 0.7). The relationship between anaerobic heat production rate and bivalve body size is different with a b = 1.0 (Pamatmat 1979). In general, anaerobic metabolism for intertidal mussels is about 7.5% of aerobic metabolism (Pamatmat 1979).





FIGURE 21. The general relationship between heat production, oxygen partial pressure, and aerobic, anaerobic, and total metabolism in bivalves.

Excretion Marine bivalves produce excretory waste products as a result of incomplete digestion and metabolism. Thus, various forms of carbon, nitrogen, phosphorus, and silicon can be found in the waste of bivalves. Three of these components, nitrogen, phosphorus, and silicon, are often limiting in marine environments and, for this reason, it is important that the flows and processes involving these constituents be understood (see Chapter 6). While metabolic degradation of organic compounds takes place in all living tissues, the excretion of the end products of metabolism usually takes place via the kidneys and across tissue surfaces, particularly the gills. Both of these locations have high surface-to-volume ratios that allow maximum exchange across their surfaces. It has long been thought that filtration of the blood occurs in the pericardial coelom of bivalves, and the products of this filtration flow to the kidney where secretion and reabsorption take place (Martin and Harrison 1964). Bivalve molluscs excrete nitrogen as a major endproduct of protein and nucleic acid metabolism. In studies using incubation chambers, ammonium is the major excretory product with urea, uric acid, purines, and free amino acids (FAA) in lesser amounts (Hammen 1980). However, recent studies using high performance liquid chromatography (HPLC), a technique that directly measures the net fluxes of metabolites during a single passage of natural sea water over a bivalve’s gill, have shown © 1996 by CRC Press LLC




that ammonia is the only nitrogenous waste product excreted by some bivalves (Hawkins and Bayne 1992). TABLE 4 Representative Percent of Total Nitrogen of Specific Excretion Products By Selected Marine Bivalves %N Species Crassostrea virginica Donax serra Donax sordidus Mercenaria mercenaria Geukensia demissus Mytilus edulis Mytilus galoprovincialis Solemya velum Tagelus plebius Teredo navalis

NH4

Urea

FAA

Uric Acid

Ref.

68 77 78 66 64 67–41 58–37 70 50 55

8 2 1

21 21 22 30 36 55 42–63 27 31 10

3

Hammen 1980 Cockroff 1990 Cockroff 1990 Hammen 1980 Hammen 1980 Bayne and Scullard 1977 Bayne and Scullard 1977 Hammen 1980 Hammen 1980 Hammen 1980

4

4

3 19 35

As noted above, incubation techniques indicate that ammonia is the most common nitrogenous excretory product, varying from 37 to 78% of total nitrogen excreted by bivalves (Table 4). Some of the ammonia produced within the bivalves’ tissues may be utilized to synthesize organic products, but there is always a surplus that is excreted to the external environment. It is unclear at this time whether the FAAs observed in incubation studies are the actual products of bivalves or other heterotrophs in the water of the chamber. At the ecosystem level of investigation, FAAs are often referred to as DON, or dissolved organic nitrogen. Bayne et al. (1976) note that the rates of nitrogen excretion are extremely variable, and this variability is probably due to marked seasonal changes in nutrient storage and utilization of reserves. There is evidence that organism size and feeding status together with environmental temperature, salinity, and exposure to air can all influence the rate of nitrogen excretion. As with oxygen consumption, nitrogen excretion increases with bivalve size according to the following equation: N = aWb where N is the rate of nitrogen excretion, W is the weight of the body and a and b are coefficients (Hammen 1980). Normally, during starvation bivalves metabolize stored glycogen, but as these reserves are used up, they are forced to increase protein catabolism as a source of energy (Bayne et al. 1976). In Mytilus edulis, ammonia excretion rises with temperature, but there is no acclimation (Bayne and Scullard





1977). Numerous investigators (see Bayne et al. 1976) have found that the rate of ammonia excretion increases as salinity decreases. These observations are supported by a review by Griffiths and Griffiths (1987) that found that the coefficients of the excretion–size relationship are strongly influenced by size, temperature, salinity, and exposure.

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4

Population Processes

INTRODUCTION A group of organisms of the same species living in the same area is termed a population. Each population has a number of characteristics that can be categorized as biological or group attributes. Biological attributes are characteristics the population shares with its component organisms. Life history or cycle is most often given as a biological attribute because a population grows, differentiates, and maintains itself just like individual organisms. Group attributes are common only to the population and include birth rate (natality), death rate (mortality), and age structure. These group attributes are unique to the population and only have meaning to a population of organisms (Odum 1983). These population or group attributes reflect the ecology of a species and can provide information on the spatial and temporal aspects of the environment (Cerrato 1980). In this chapter, the demography of bivalve populations will be presented by examining life tables of specific bivalves and by exploring a number of population processes, i.e., growth, recruitment, and mortality, for a variety of species. As all of these processes influence the production of bivalves, understanding them is vital to determining the role of these animals in ecosystems.

LIFE CYCLE The life cycle of bivalve molluscs begins with fertilization of eggs, usually in the water surrounding the adults. Gametes are typically shed within the shell cavity and swept out on the exhalant currents generated by pumping. In contrast, some bivalves brood their eggs, with fertilization occurring in the mantle cavity. Here again the bivalve water pump is important in bringing in the sperm for fertilization. In shipworms, brooding occurs in the suprabranchial cavity, and in the oyster, Ostrea, within the gills (Barnes 1974). The eggs of bivalves develop into free-swimming trochophore and then veliger larvae. In some marine bivalves, the veliger stage may last as long as several months. In others, it is only a few days. In brooders, the veliger larvae are released after a specific period (8 days in Ostrea edulis). The larval stage is planktonic and subject to very high mortality. At metamorphosis, the larvae settle out of the plankton and the bivalve spends its remaining life as a member of the benthos. Consequently, the life cycle of a marine bivalve can be separated into two very distinct stages, the planktonic presettlement–larval period and the post settlement juvenile–adult period. The presettlement period is important for dispersal of the species, while the juvenile–adult period is important for reproduction. The two stages are spatially and





temporally separated for most of their existence, and that reduces the chances of adult induced mortality on the larvae through adult filter feeding. The population dynamic of the presettlement stage is poorly studied, probably because of its short duration and the greater logistical complications of sampling plankton. Thus, most studies of bivalve population dynamics focus on the postsettlement stage and particularly on shallow water, commercially valuable species.

STATISTICAL MEASURES OF POPULATIONS Postsettlement bivalves are excellent subjects for population studies because their shells provide a long lasting record of the organism’s life and, through statistical compilation, the dynamics (demography) of a given population. The shell is an easily observed and identified characteristic of a bivalve species and collections of living animals can yield accurate estimates of population density (Cerrato 1980). In some cases, shells from ancient deposits can also be used to determine the densities and other properties of past populations of bivalves (Rhoads et al. 1982; Powell et al. 1984). Through shell growth rings, the growth rate and age of individual bivalves can be assessed. This information can be compiled to determine age structure for a specific population. In some cases, the shell records tell-tale clues as to the causes of mortality. Not all population parameters can be determined from the shell. Fecundity requires the analysis of living bivalves, while incidences of disease and parasitism may require direct observation of living tissues.

DENSITY Often the simplest population attributes to determine are density and abundance. Generally, density refers to the population size at a given time, i.e., number of individuals per unit area, while abundance implies a dynamic (changing) aspect to the population, i.e., number per unit area per unit time. Because the individuals in a population vary physiologically and genetically and respond differently to the environment, it is usually more meaningful to focus on the population at a level of resolution greater than simple density. Density observations on a population are easily arranged into nonoverlapping groups or classes that divide the life span or size range of the organism. The class frequencies for the data are found by summing the number of individuals in each class. The class frequency data may appear as a table or more often as a histogram with classes (size or age) plotted versus frequency (Figure 22). In bivalves, age is often used in these plots, as growth or age can be clearly determined from rings on the shell. If small size class intervals are used in constructing the histogram, variations in growth within a year or recruitment class can be resolved (Cerrato 1980). Most temperate and boreal shallow water bivalves are seasonally programmed with distinct spawning periods. With frequent sampling, these spawning periods will be reflected in the size frequency histograms as a pulse of new individuals at the smallest size class. Normally, the smaller size or year classes make up the numerical majority of the population while the older and larger classes are only a small portion © 1996 by CRC Press LLC




FIGURE 22. Size-frequency distributions of the cockle Cerastoderma in Ireland. (Adapted from Seed, R. and Brown, R.A. 1975.)





of the total population size. If additional samples are taken through time, these samples will show recruitment pulses migrating across successive size frequency plots. This movement across the frequency plots is caused by the growth of individuals within the population and offers a way of computing modal or average growth for a size class (see Chapter 3). Mortality will also cause the pulse to decrease in height or shrink and it too can be estimated from the size frequency plot (see Figure 22). For long-lived species, multiple pulses are often discernible in the size frequency histogram, and each pulse represents an age class or year class in the population. It is also common for an age class or pulse to have a roughly normal distribution and to overlap adjacent age classes. There are a number of graphical and statistical methods (Walford 1946; Cassie 1954; Sheldon 1965; Cerrato 1980; Basson et al. 1988) that can be used to separate the overlapping age classes. Thus, the size frequency histogram contains valuable information about the population in question, over and above simple measures of density.

REPRODUCTION The process of reproduction is the generation of new individuals that have the potential to become members of the population. Reproduction is integrated into the bivalve’s life cycle and is one of the few instances where the planktonic gamete and larval stages are linked to the postsettlement juvenile and adult stages. There are a number of terms that are often used and confused when discussing reproduction in bivalves at the population level, and they need to be specifically defined (after Krebs 1978). Fecundity is the potential capability of an organism to produce reproductive units. Fertility is the actual capability for an organism to produce offspring. Natality or birth rate is the rate of production of new individuals by a population. Reproductive output is the amount of gametes released into the environment. Settlement is the process by which individual bivalve larvae come into contact with and attach to the bottom (usually permanently). Recruitment is the successful colonization of the bottom by bivalves and implies the passage of time with survival and postsettlement mortality (Seed and Suchanek 1992). The reproductive output in many bivalves can represent a major proportion of total population production and can be a significant energy input to the water column. Most bivalves are iteroparous (multiple breeding in a lifetime) and their reproductive output varies according to size or age, with smaller individuals putting proportionally more effort into somatic growth and older individuals putting more effort into reproduction (Bayne 1976). Therefore, younger individuals as a group may contribute as many or more offspring because their numbers are usually much greater than © 1996 by CRC Press LLC




those of larger individuals in the population. This change in reproductive output with age appears to be the rule not only for energy and carbon, but also for nitrogen (Rodhouse et al. 1984). Reproductive output or gamete production in most bivalves seems to follow the planktotrophic strategy (Vance 1973; Bayne 1976) that is characterized by high fecundity and high metabolic cost. A cursory survey of estimated bivalve reproductive effort as a proportion of total production is given in Table 5. Clearly, reproductive effort is highly variable both within and among species. While most low values can be related to young populations, those values for Crassostrea and Geukensia are for mature populations. However, these populations are in the mid- to upper intertidal zone in the subtropical U.S. marsh–estuarine ecosystems where stress due to exposure may detract energy from reproductive effort. Changes in year-to-year environmental conditions may also explain variations in population reproductive effort in Tellina, Choromytilus, and Perna. TABLE 5 Bivalve Reproductive Effort in Relation to Total Production (%) Reproductive Effort (%)

Species Aulacomya ater Chione cancellata Choromytilus meridionalis Crassostrea gigas Crassostrea virginica Dosinia elegans Geukensia demissa Lyrodus pedicellatus Mercenaria mercenaria Ostrea edulis Patinopectin yessoensis Perna perna Scrobicularia plana Tellina tenuis

63 50 73 98 16 47 17 47 46 47 3–38 16 24–52 9–62

Ref. Griffiths and Griffiths 1987 Moore and Lopez 1969 Griffiths 1981 Bernard 1974 Dame 1976 Moore and Lopez 1970 Kuenzler 1961 Gallager et al. 1981 Hibbert 1977 Rodhouse 1978 Fuji and Hashizuma 1974 Berry 1978 Hughes 1970 Trevallion 1971

POPULATION GROWTH The size of a population in terms of numbers is a function of the inputs and outputs to that population. B

D N t

I




E


The major inputs or additions to the population are the births of new individuals (B) and immigration (I), while the major losses or outputs are death (D) and emigration (E). The size or density of the population is Nt. The change in population size (∆N) per unit change in time (∆t) can be represented by: ∆N = B + I − (D + E ) ∆t

From an ecosystem perspective, it is probably more meaningful to represent these parameters as biomass in units of energy or grams of material, i.e., carbon, nitrogen, or phosphorus (Valiela 1984). When a population exists in a favorable environment with no limitations due to space, food, predation, or environment, the specific growth rate (growth rate per individual) of the population is constant and maximal for the specific conditions. This growth rate is specific for a particular population age structure, as found in a size class histogram, and is a size index of population growth (Odum 1983). This growth is represented by r, a coefficient in the exponential growth model: dN = rN dt

and where r = dN( Ndt )

or when integrated Nt = Noert Where Nt is the population size at some later time t, No is the population size at the initial time, e is the exponential constant and r is the growth coefficient. Taking the natural logarithm of the preceding equation ln N t = ln N o + rt

and r=

ln N t − ln N o t

The index r is, then, the difference between the instantaneous specific birth (natality) rate b and the instantaneous death (mortality) rate d. When emigration and immigration are small or nonexistent, as is the case with most bivalves, then they can be ignored and © 1996 by CRC Press LLC




FIGURE 23. The relationship between reproductive value and age for r values for the clam Mya arenaria. (Adapted from Brousseau, D.J. 1978.)

BIVALVES AS OPEN OR METAPOPULATIONS As the spatial scale for considering a population increases, the population dynamics are less affected by movements (immigration and emigration) and become increasingly dominated by the interactions of birth and death rates discussed above (McGrorty and Goss-Custard 1991). With organisms that have a great potential for dispersal, e.g., marine bivalve larvae, enormous geographical areas must be considered in order to achieve the birth rate and death rate control of population dynamics. This requirement is usually impractical. Instead of this closed or entire population approach, the combined population properties of many local groups (patches, subpopulations, etc.) or metapopulations can be utilized and depends not only on the interaction between groups (Roughgarden et al. 1985) but also within group processes of density-dependent mortality, self-thinning, density-limited growth, and density-dependent emigration (McGrorty and Goss-Custard 1991). With this approach, the distribution, size, and density of the metapopulation may be regulated or limited by the supply of larvae from the plankton rather than by local fecundity (McGrorty et al. 1990). In a field study of the population dynamics of Mytilus edulis in the Exe estuary, England, McGrorty et al. (1990) and McGrorty and Goss-Custard (1991) found that annual variations in spat fall over the entire estuary were related closely to the densities of adults on the different beds. They further found that the main environmental gradient along which the population dynamics of mussels in this estuary survived was exposure time. Mortality regulation during the first year resulted in a pronounced stability of the total population. © 1996 by CRC Press LLC




LIFE AND FECUNDITY TABLES The age-specific statistical characteristics of mortality, survivorship, and life expectancy are generally represented in columnar form in a life table. Because the size of a population may change as a function of births and deaths of individuals, the life table provides an organized method for determining these properties. The life table is made up of rows and columns of both observed and calculated information on a population. The rows usually represent the age or year classes, while the columns denote various population properties. Definitions and calculations for the columns are given in Table 6. While the number of individuals alive at a particular time (nx) is directly observed, mortality can be obtained from age of death observations by computing the decline in the numbers of individuals in an age class through time and by directly monitoring the death rate of marked individuals (Cerrato 1980). It is normal to analyze mortality by focusing on one property, lx, the survivorship. Usually the log of survivorship is plotted as a function of age (x). Although there are several standard survivorship curve forms, Kurten (1964) has pointed out that when the complete life cycle of a species is considered, the shape of the survivorship curve is sigmoidal, with high mortality in both young and old age classes (Figure 24).

FIGURE 24. A survivorship curve for the clam Mya arenaria at Gloucester, MA. (Adapted from Brousseau, D.J. 1978.)

A classical example of a bivalve life table is given in Table 7. In the Pismo clam, Tivela stultorum, the numbers of observed living clams in a given age interval are adjusted to an initial cohort of 1000 juvenile clams. Of this initial cohort, 550 clams die during the first age interval (dx) and can be expressed as a mortality rate © 1996 by CRC Press LLC




TABLE 7 Life Table for Tivela stultorum, the Pismo Clam Age X (years) 0–1 1–2 2–3 3–4 4–5 5–6 6–7 7–8

lx

dx

qx

Lx

Tx

ex (years)

1000 450 248 176 116 56 18 5

550 202 72 60 60 38 13 5

550 449 290 341 517 678 722 1000

723 349 212 146 86 37 11.5 2.5

1569 844 495 283 137 51 14 2.5

1.57 1.87 1.99 1.60 1.18 0.90 0.75 0.50

After Cerrato, R.M. 1980.

(qx) of 550/1000 or 0.550. The average number of clams alive during the age interval (Lx) is 723 or (1000 + 450)/2. Summing the Lx column from the bottom yields the Tx value, and dividing this by lx gives the life expectancy in years (ex) for each age interval. The data show that young (0 to 2) and older (4 to 8) age interval clams die more rapidly than middle-aged clams. Life expectancy is highest for 1- 3-year-old clams. These observations are typical for invertebrate populations that do not brood or protect their young and experience high mortality after settlement. An excellent example of a life table with fertility computations for a marine bivalve, Mya arenaria, is given by Brousseau (1978) and is described in Table 8. The data in this table are presented differently than those in Table 7 in that the proportion of clams surviving (lx) is used rather than observed numbers and the first three year classes were subdivided. This life table (Table 8) shows that Mya reaches maximum life expectancy at 30 mm length or about an age of 1 year. Mortality as described by survivorship is highest for larvae and very old size classes (Figure 24). This survivorship curve form is sigmoidal as suggested by Kurten (1964), and supports Murphy’s (1968) theory that long life and iteroparity are favored under conditions where spawning or settlement success are highly variable. Using histological analysis, Brousseau (1978) also was able to compute age-specific fecundity. This property increased with size and age from 40 mm and 1.7 years with a fecundity of 7399 and to a maximum age and size with a fecundity of 72,125 or an order of magnitude higher than the younger clams. Using her estimates of lx and mx, Brousseau (1978) was able to compute a very high intrinsic rate of natural increase (rmax) of 4.74 for this clam population. This enormous potential for increase is completely offset by high larval mortality, i.e., in the order of 0.001 to 0.0001% of larvae spawned eventually settled (Brousseau 1978). As we have seen in the size frequency histograms, new recruits to the bivalve population show up as pulses of individuals in the smallest size or year classes. Powell et al. (1984) have shown that if the sample frequency is too long the





TABLE 8 Mya arenaria Life and Fecundity Table Size class (mm)

Age x (years)

lx

Lx

ex (years)

qx

mx

2.0–4.9 5.0–9.9 10.0–14.9 15.0–19.9 20.0–24.9 25.0–29.9 30.0–34.9 35.0–39.9 40.0–44.9 45.0–49.9 50.0–54.9 55.0–59.9 60.0–64.9 65.0–69.9 70.0–74.9 75.0–79.9 80.0–84.9

0.143 0.286 0.428 0.571 0.714 0.857 1.000 1.333 1.667 2.000 2.333 2.666 3.000 4.000 5.000 6.000 7.000+

0.557 0.662 0.800 0.800 0.834 0.900 0.968 0.978 0.963 0.966 0.973 0.962 0.952 0.949 0.969 0.984 0.911

0.610 0.731 0.800 0.817 0.867 0.934 0.973 0.971 0.965 0.970 0.968 0.957 0.951 0.959 0.977 0.948

0.769 1.820 3.562 4.602 6.336 8.248 9.178 8.758 8.143 7.758 7.268 6.665 6.186 5.794 5.386 4.690 3.830

0.885 0.675 0.400 0.400 0.333 0.199 0.062 0.045 0.075 0.066 0.055 0.078 0.098 0.101 0.059 0.031 0.176

— — — — — — — — 7,379 13,589 — 18,835 33,605 36,624 46,034 56,986 72,125

After Brousseau, D.J. 1978.

abundance of newly settled recruits will not be estimated accurately. This is because most juvenile bivalves recruited to the benthic population may settle, live, and die between sampling periods and thus, not be included in the size or age frequency histogram. These authors found that by sampling the shells of bivalves in the sediments adjacent to the live population, they could construct the death assemblage of the population. Input into the short-term death assemblage occurs in pulses and these pulses gradually decay as a result of taphonomic processes that destroy the individual shells. If larval settlement produces pulses of juveniles, if pulse decay rates are low, and if the half-lives of the decaying pulses are known, then the size of the original settlement can be determined from the death assemblage. From this analysis, Powell et al. (1984) determined that larval settlement is consistently underestimated by as much as 90% from living population data on bivalves.

MORTALITY As noted earlier, the height of the age size class histograms in postsettlement bivalves decreases in size as mortality reduces population size. Mortality is also explicit in the plot of survivorship vs. time. Mortality in bivalves is caused by abiotic factors, predation, disease, and competition and human harvest for food or other products.





ABIOTIC MORTALITY As discussed in Chapter 2, physical factors limit the existence of a bivalve to a given environment or niche. For bivalves, the most important of these abiotic mortality agents are temperature, aerial exposure, salinity, oxygen concentration, siltation, and waves. Depending on the latitude and coastal morphology, many of these factors may vary seasonally and, thus, result in seasonal mortality effects. In addition, many physical factors may act in concert with other factors to cause mortality. At the extreme, catastrophic environmental events, e.g., storms or widespread anoxia, may lead to mass mortality in bivalve populations. Temperature can be a major cause of mortality in the intertidal zone. Summer extremes of high temperature during daytime low tide exposure can lead to extensive mortalities, particularly in subtropical and tropical populations of oysters (Dame 1976) and mussels (Suchanek 1978; Tsuchiya 1983), while extreme cold and icing conditions can do likewise in northern temperate and boreal bivalve populations (Suchanek 1986). Strong waves associated with storms can dislodge intertidal bivalves, resulting in mortality. Such conditions may also bring large floating debris, i.e., logs, that batter, crush, and dislodge bivalves in rocky shallow and intertidal environments (Dayton 1971; Lubchenco and Menge 1978; Suchanek 1986). In unconsolidated sedimentary environments, shifting of particles, burial, erosion, and direct movement of bivalves by currents and waves can also cause patchiness. Anaerobic conditions are common to shallow bays and estuaries with poor circulation. Although some bivalves, e.g., oysters, can close their valves and resist anaerobic conditions for weeks, others (e.g., mussels) may suffer immediate mass mortality. For example, in the Dutch Oosterschelde estuary, large populations of mussels are cultivated. If the storm surge barrier separating the estuary from the North Sea is closed, water circulation is greatly reduced and the large population of mussels may rapidly drive the system to an anaerobic state and result in mass mortalities of mussels.

PREDATION Often the most important cause of mortality in bivalve populations is predation. Predation can be defined as (a) the process that occurs when one organism kills another for food, or (b) when individuals of one species eat living individuals of another, or (c) a process by which one population benefits at the expense of another, or (d) any ecological process in which energy and matter flow from one species to another (Taylor 1984). For our purposes, predation is a direct interaction between different species populations. In bivalve-dominated systems, the most common predators are gastropods, starfish, crabs, fish, birds, and mammals. Rather than be controlled by a specific predator, most sessile and slow-moving bivalves are usually preyed upon by suites or gilds of predators (Seed 1993). Many bivalve predators are only effective on certain size classes of prey, usually the smaller sizes, and at specific seasons of the annual cycle. Methods of predation range from defeating the defenses of the bivalve shell by small invertebrates and some birds, to crushing or breaking the shells by crabs, fish, and © 1996 by CRC Press LLC




mammals, to the swallowing of the whole bivalve by birds. Most of our information on the predation of bivalves comes from intertidal and shallow water environments and is usually focused on economically important species. Those interested in a detailed review of the influence of invertebrate predators on bivalves should see Seed (1993) and of birds, Meire (1993). Because bivalve larvae live in a different habitat, they suffer predation from an entirely different group of predators than do the benthic adult stages. The most commonly reported bivalve larval predators are ctenophores and jellyfish. In the bays along the Atlantic coast of North America, for example, the ctenophore Mnemiopsis leidyi has been deduced to be a major planktonic predator of oyster larvae as the ctenophore’s density is inversely related to that of the oyster larvae (Kremer 1979). Curiously, this ctenophore is also preyed upon by the sea nettle, Chrysaora quinquecirrha, which is also a major predator of oyster larvae in Chesapeake Bay (Cargo and Shultz 1967). In addition to these truly planktonic predators, benthic adult bivalve filter feeders may also ingest bivalve larvae (Korringa 1949). Although the idea that there is a significant interaction between established adult bivalve filter feeders and their settling larvae has been strongly questioned by Black and Peterson (1988), field manipulation studies with dense populations of the cockle, Cerastoderma edule, suggest that adult–larval interactions play an important role in this species population dynamics (Andre and Rosenberg 1991; Andre et al. 1993). Studies by Möller (1986) suggested that plots with high densities of Mya arenaria had fewer settled juveniles of M. arenaria and C. edule than control plots with low densities of M. arenaria. Andre and Rosenberg (1991) concluded that the settlement of bivalve larvae may be reduced by up to 40% in the presence of adult C. edule and M. arenaria. In a follow-up study using an experimental flume, Andre et al. (1993) determined that adult C. edule reduced the settlement of C. edule larvae by 33% in an area immediately surrounding individual adults. They also found that over dense beds of these cockles, as many as 75% of the observed larvae were inhaled by adults. These authors concluded that for C. edule beds the reduction in larval settlement was small to moderate at the scale of the individual adult, but that inhalation of settling larvae by the populations of resident filter feeding bivalves may cause a significant decrease in settlement on a larger scale (10 to 1000 m). Thus, when spatial and temporal scaling are taken into account, it appears that dense populations of adult bivalve filter feeders can be and are a major cause of mortality for settling larvae. Compared to the predation of planktonic larvae, the predation of postsettlement bivalves is better studied because of the accessibility of the prey. The predators range in size from small flatworms to mammals. Rather than conduct a comprehensive review of bivalve predators (see Seed 1993 and Meire 1993), I shall provide a synopsis of the major players and give examples where appropriate. The flatworm, Stylochus ellipticus, is an important predator of newly settled oysters on the Atlantic coast of North America (Loosanoff 1956 and Webster and Medford 1959). Stylochus appears to enter the oyster spat through the slightly opened valves where it then eats the soft body tissues. Although this flatworm seems to prefer barnacles, it will switch to oysters when they are abundant. Similar findings have been reported for Stylochus mediterraneus in mussels (Galleni et al. 1977). © 1996 by CRC Press LLC




Gastropod molluscs are common predators of bivalves. The majority of gastropod predators drill holes in the bivalve shell by a combination of mechanical (radula) and chemical means. These predators are often opportunistic, switching between prey species of bivalve or other phyla, e.g., barnacles, depending on prey availability and ease of successful attack. These predators also seem to favor younger or thinner shelled bivalves over older or thicker-shelled prey (Seed 1993). While most gastropod predation studies focus on temperate economically important bivalve species, i.e., clams, mussels and oysters (Galtsoff 1964; Seed 1992, 1993), studies of the cultivated tropical clam, Tridacna maxima, in the Cook Islands of the Pacific also reflect high gastropod predation on the smaller size classes (

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